Non-Target Insects and Beneficial Species
Impact of Pesticides on Non-Target Insects and Beneficial Species
Non-target and beneficial species can be impacted by pesticides through direct or indirect routes, such as water contamination and runoff, pesticide residues, and by consuming food that has been sprayed.
- A 2014 study published in Chemosphere examined the effects of different pesticides on a common insect predator.
- Researchers found that exposure to some pesticides were lethal, while exposure to others led to a decrease in plant feeding time and reduced predation rates.
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A study on non-target molluscan herbivores and their insect predators found that neonicotinoid seed-treated soy beans can unintentionally impact predatory, beneficial insects through a previously unexplored pathway.
Chlaenius tricolor, beneficial beetle - Soy beans were treated with the neonicotinoid thiamethoxam.
- The seed treatments had zero effect on pest slugs, and instead were bioaccumulated and then transferred through the slugs into their insect predators, impairing or killing >60%.
- This resulted in a loss of crop due to a decline in beneficial insect predators and an increase in pest slug population.
[See More Scientific Studies Below]
Economic Cost
The European Academies' Science Advisory Council (EASAC) estimates global natural pest control to be worth $100 billion annually. Natural pest control is where insects consume pests so that chemicals are not necessary. It focuses on encouraging predatory insects to consume pests, which is a least-toxic approach that is undermined through chemical usage by destroying the balance that exists within a predator-prey relationship.
Non-target insects also act as a food source for animals that bring in a substantial amount of revenue. US citizens spend over $60 billion annually on hunting, fishing and observing wildlife, much of which is dependent on insects as a food source. Researchers have found that there is a steady decline in these insects due to pesticide exposure and an overall decline in biodiversity. It could be concluded then that, as beneficial insect populations decline, their ability to provide ecosystem services will also decline, impacting the available wildlife for hunting, fishing, and observing. The demand for these recreational activities will stay constant while the supply (availability) will decline, causing an increase in dollars spent by US citizens for each year.
Litigation & Lawsuits
See our Pollinators and Soil Biota pages.
What Can You Do?
- Learn about the Hazards and Alternatives to using lawn pesticides.
- Go Organic – Visit our Eating with a Conscience page to learn why eating organic foods is the right choice.
- Visit our Tools for Change page to learn how to organize your community against pesticide use.
- Sign up for Beyond Pesticides’ Action Alerts to stay up-to-date on the latest petitions and news.
Scientific Studies:
Predatory soil arthropods are under-represented in insecticide toxicity studies, severely limiting our understanding of how insecticides affect soil-invertebrate communities in agroecosystems. As a step toward addressing this issue, we conducted novel acute oral, topical, and soil-based toxicity assays on 9 ground beetle species (Coleopetera: Carabidae) in response to the neonicotinoid insecticides clothianidin, thiamethoxam, and imidacloprid. From these assays, we calculated 24 h TD50, TC50, LD50, and LC50 values, measured 24 h feeding activity, and recorded beetle survival for 7 d after exposure.
[Pearsons, K. and Tooker, J. (2025) Acute toxicity of neonicotinoid insecticides to ground beetles (Coleoptera: Carabidae) from Pennsylvania, Environmental Entomology. Available at: https://academic.oup.com/ee/advance-article-abstract/doi/10.1093/ee/nvaf048/8128784.]
Chlorothalonil, a widely used fungicide in agriculture, has raised concerns regarding its impact on non-target species. This study examined the effects of chronic chlorothalonil exposure on larval development and reproductive performance of the vinegar fly, Drosophila melanogaster. Drosophila eggs were reared on a diet supplemented with sublethal concentrations of chlorothalonil (5–120 mg kg−1). Larval pupation was measured as an indicator of survival and growth, while fecundity, ovariole count and body weight served as proxies for female reproductive performance. A ferrozine assay was used to examine mitochondrial mitoferrin activity in males as a reproductive marker related to iron metabolism. Chlorothalonil exposure decreases larval survival, extends developmental duration and reduces fecundity. Even at the lowest tested concentration, chlorothalonil exposure resulted in reduced body weight, ovariole count and egg production compared with non-exposed individuals. Male flies also demonstrated reduced iron levels. These findings underscore that chronic, sublethal chlorothalonil exposure not only induces larval mortality but also adversely affects fecundity in adult insects. Assessing the toxicological effects of agrochemicals on non-target organisms is critical to understanding the broader environmental impacts of these substances. Such insights are vital for developing conservation strategies that safeguard ecosystems and support biodiversity while promoting sustainable agricultural practices.
[Dissawa Darshika M., Boyer Ines and Ponton Fleur 2025 Chlorothalonil exposure impacts larval development and adult reproductive performance in Drosophila melanogaster R. Soc. Open Sci.12250136 http://doi.org/10.1098/rsos.250136]
Decisions on whether and how to manage introduced species can be controversial, but public attitudes towards introduced species management (ISM) are poorly understood. Despite the potential disruptive impacts of such controversies on public relations and conservation goals, decision-makers are currently left with little information on the social acceptability of different management alternatives. To better understand the social acceptability of core features of ISM in the United States, we conducted an online experiment with vignettes describing hypothetical but realistic ISM scenarios, varying targeted taxon (insect or plant), control method (mechanical, chemical and biological), risk severity (low and high) and type of non-target risk (to humans or native species). Not surprisingly, management with low risk was most acceptable, particularly for mechanical control. In high-risk scenarios, only mechanical control was acceptable, but only by a slim majority of respondents. Overall, chemical and biological controls showed low levels of acceptability. Surprisingly, there was no significant difference in how respondents ranked risks to people and risks to native species. Beyond differences in acceptability between management factors, we also find that the acceptability of management and attitudes towards risk were associated with respondents' demographic characteristics. Policy Implications. Overall, our findings indicate that widespread acceptability of ISM should not be assumed. While management activities representing low-risk scenarios find some support in the public, our results highlight a disconnect between the effectiveness of common management methods and their social acceptability. Our findings highlight the need for evidence-guided ISM, which includes evidence of harmful impacts of introduced species, as well as risks and benefits of management activities, as one potential way to increase the social acceptability of non-native species management.
[Simmons, W. et al. (2025) Common approaches to introduced species management face widespread acceptance problems in the United States, People and Nature. Available at: https://besjournals.onlinelibrary.wiley.com/doi/am-pdf/10.1002/pan3.70053.]
Pollinators face declines and diversity loss associated with multiple stressors, particularly pesticides. Most pollination services are provided by annual bees that undergo winter diapause, and many common pesticides are highly soluble in water and move through soil and plants where bees hibernate and feed, yet the effects of pesticides on pollinators’ diapause survival and performance are poorly understood. Pesticides may have complex effects in bees, and some were shown to induce hormetic effects on various traits characterized by high-dose inhibition coupled with low-dose stimulation. Here, we examined the occurrence of hormesis in the responses of bees to imidacloprid. We found that while longevity and reproduction were reduced following exposure to imidacloprid, the survival length of new queens (gynes) was greater. Diapause is a critical period in the life cycle of most bees with profound effects on their health. Exposure to sublethal doses of pesticides may increase bees’ resistance to stress/cold during diapause but may also trade off with reduced reproductive performance later in life. Identifying these trade-offs is crucial to understanding how stressors affect pollinator health and should be accounted for when assessing pesticide risk, designing studies and facilitating conservation and management tools for supporting annual bees during diapause.
[Amsalem, E., Derstine, N. and Murray, C. (2025) Hormetic response to pesticides in diapausing bees, Biology Letters. Available at: https://royalsocietypublishing.org/doi/full/10.1098/rsbl.2024.0612.]
Among the most immediate drivers of American burying beetle (Nicrophorus americanus Olivier) declines, nontarget toxicity to pesticides is poorly understood. Acute, episodic exposure to neonicotinoid insecticides at environmentally relevant concentrations is linked to negative impacts on beneficial terrestrial insect taxa. Beyond mortality, behavioral indicators of toxicity are often better suited to assess sublethal effects of residual concentrations in the environment. First, Nicrophorus spp. congeners were used to generate and identify a low-dose exposure rate (lethal dose 10%; LD10) from an acute, 24-hour exposure and the concentration-series was confirmed by LC–MS/MS. Next, we evaluated the effects of single and repeated low-dose (LD10 = 58.9 ng/beetle) imidacloprid exposure on N. americanus behavior (10 minutes post-dose) and mortality (10 days post-dose). Behavior parameters were analyzed using EthoVision-XT. Control N. americanus were significantly less mobile, demonstrating death-feigning, an anti-predator behavior. Single LD10 dosed N. americanus were hyperactive, traveling over 4 times farther (total distance; p = 0.03) and faster (mean velocity; p = 0.02) than controls. Single and repeated LD10 dosed N. americanus extended their wings without taking flight and flipped on their backs. All control N. americanus survived 10 days post-dose; single LD10 and repeated LD10 exhibited 30% and 50% mortality, respectively. A single LD10 exposure event was sufficient to significantly elicit greater movement and high predation risk behaviors, whereas repeated LD10 exposure did not worsen behavioral impairment but increased mortality over time. Collectively, generalized linear mixed effects models indicated that distance traveled, velocity, and extended wings were significant predictors of mortality. Recently reclassified, the federally threatened N. americanus may be at greater risk to insecticide exposure than previously thought and vulnerable to episodic, low-dose neonicotinoid exposure.
[Cavallaro, M. et al. (2025) Neonicotinoid exposure causes behavioral impairment and delayed mortality of the federally threatened American burying beetle, Nicrophorus americanus, PLOS One. Available at: https://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0314243.]
Although pesticides have been proposed as one of the main causes of insect decline, there are still few studies assessing their effects on non-target species under field conditions. Here we investigated the effects of the neonicotinoid insecticide Mospilan®SG (active ingredient acetamiprid) on plant bugs (Heteroptera: Miridae), a dominant group of European grassland insect communities. In a controlled field study, the abundance of three focal species was reduced by up to 92% two days after field exposure at concentrations expected at field margins, with mortality varying among species. Follow-up feeding assays with insecticide-treated host plants in the greenhouse and controlled dose-response laboratory assays confirmed the strong negative effects on non-target species. Strikingly, when comparing the lethal dose 50 derived from Mospilan®SG with a value reported for honeybees using another acetamiprid formulation, the insecticide was over 11,000 times more toxic to plant bugs than to honeybees. In addition, males were 20 times more sensitive than females in the two tested species. Thus, continuous exposure to this neonicotinoid may reduce plant bug populations and promote insecticide-tolerant species, altering community composition. We suggest that sex-specific sensitivity be considered in risk assessment and conclude that the true risk to non-target insects is currently greatly underestimated.
[Sedlmeier, J.E. et al. (2025) Neonicotinoid insecticides can pose a severe threat to grassland plant bug communities, Communications Earth & Environment. Available at: https://www.nature.com/articles/s43247-025-02065-y.]
During the past decades, insect diversity, abundance and biomass has decreased throughout Central Europe, mainly due to agricultural intensification. Organic field management aims to counteract this negative trend. In order to investigate the effects of farming intensity on insect diversity, abundance, and biomass, we sampled insects from 2021 to 2023 on three organically and three conventionally managed meadows in southern Germany using Malaise traps. All individuals collected were subsequently analysed using metabarcoding, and BINs were determined. All identified taxa were then classified according to their characteristics and performance during the developmental and adult stage. All bulk samples were dried and weighted for the determination of biomass. BIN diversity of flying insects was 11% and biomass 75% higher on organically managed meadows compared to conventional ones. Although all functional guilds were more diverse on organic meadows, species overlap between management types was moderate and ranged from 60 to 76%, indicating that both, conventional and organic meadows harbour specific and species rich insect communities. Our trait-analyses showed that both habitat structure as well as resource availability strongly impacted the occurrence of species and diversity. The observed differences in diversity mainly result from the higher mowing frequency applied to conventionally managed meadows. Our study highlights that organic and conventional farming both have potential to maintain a high insect diversity and biomass in agricultural landscapes if some basic prerequisites for population survival are fulfilled.
[Habel, J. et al. (2025) Organic farming fosters arthropod diversity of specific insect guilds – evidence from metabarcoding, Conservation Genetics. Available at: https://link.springer.com/article/10.1007/s10592-025-01707-0.]
Since the 1980s, monarch butterfly (Danaus plexippus plexippus) populations across North America have declined by 80–95%. Although several studies have implicated pesticides as a contributing factor to their population declines, our understanding of monarch exposure levels in nature remains limited. In January 2024, a mass mortality event near an overwintering site in Pacific Grove, California, USA, provided an opportunity to analyze dead overwintering monarch butterflies for pesticide residues. Ten recently deceased butterflies were collected and analyzed using liquid and gas chromatography with tandem mass spectrometry (LC-MS/MS and GC-MS/MS). We identified a total of 15 pesticides and associated metabolites in the butterflies, including 8 insecticides (plus 1 associated metabolite), 2 herbicides (plus 2 associated metabolites), and 2 fungicides. On average, each monarch butterfly contained 7 pesticides, excluding transformation products if the parent compound was also detected. Notably, three pyrethroid insecticides—bifenthrin, cypermethrin, and permethrin—were consistently detected at or near each chemical’s lethal dose (LD50). Bifenthrin and cypermethrin were found in every sample, while permethrin was present in all but two samples. The average concentrations of these insecticides were 451.9 ng/g dry weight (dw) for bifenthrin, 646.9 ng/g dw for cypermethrin, and 337.1 ng/g dw for permethrin. These findings demonstrate pesticide contamination in monarch butterflies, including within urban areas, and highlight the risks pesticides, especially insecticides, pose to monarch populations. Additional measures may be required to safeguard this species from pesticide exposure, particularly near aggregation locations, such as overwintering sites in coastal California.
[Cibotti, S. et al. (2025) Pyrethroid insecticides implicated in mass mortality of monarch butterflies at an overwintering site in California, Environmental Toxicology and Chemistry. Available at: https://academic.oup.com/etc/advance-article-abstract/doi/10.1093/etojnl/vgaf163/8177160.]
Airborne pesticide drift poses a substantial environmental threat in agriculture, affecting ecosystems far from the application sites. This process, in which up to 25% of applied pesticides are carried by air currents, can transport chemicals over hundreds or even thousands of kilometers. Drift rates peak during the summer months, reaching as high as 60%, and are influenced by various factors, including wind speed, temperature, humidity, and soil type. Pesticide volatilization is a significant concern, occurring 25 times more frequently than surface runoff. Under certain conditions, it can result in chemical losses of compounds like metolachlor and atrazine that are up to 150 times higher. These drifting pesticides have profound impacts on biodiversity, harming non-target plants, insects, fungi, and other organisms both near application sites and in distant ecosystems. Pesticide drift has been linked to over 50% reductions in wild plant diversity within 500 m of fields, reducing floral resources for pollinators. Despite growing evidence of these effects, the long-term consequences of airborne pesticides on biodiversity remain poorly understood, especially in complex field conditions with multiple pesticide applications. Addressing this requires urgent measures, such as improved meteorological tracking during applications, adoption of biopesticides, and integrated pest management strategies. This review highlights the pressing need for research to quantify airborne pesticides' ecological impacts, advocating for sustainable practices to mitigate environmental damage.
[Albaseer, S. et al. (2024) Beyond the field: How pesticide drift endangers biodiversity, Environmental Pollution. Available at: https://www.sciencedirect.com/science/article/pii/S0269749124022437.]
Modern intensive agriculture faces a critical paradox: The very pesticides designed to protect our crops endanger essential pollinators that sustain their productivity. As human reliance on pollinator-dependent crops grows, it becomes more urgent than ever to reconcile the need for crop protection with pollinator preservation. The stakes are high, as pollinators, such as bees, are vital to food security and biodiversity.
[Rondeau, S. (2024) Digging below the surface: Hidden risks for ground-nesting bees, Science. Available at: https://www.science.org/doi/10.1126/science.adt8998.]
As agricultural production increases, the use of chemical fertilisers, herbicides, and other synthetic pesticides has equally increased over the years. Inadequate pesticide application description and monitoring has generated a heated debate among governmental organisations, agricultural industries, and conservation organisations about pesticide effects on insect species richness and abundance. This review is therefore aimed at summarizing the decline in insects’ species and individual numbers as a result of extensive pesticide utilisation and recommends possible management strategies for its mitigation. This review revealed an average pesticide application of 1.58 kg per ha per year, 0.37 kg per person per year, and 0.79 kg per USD 1000 per year. Insects have experienced a greater species abundance decline than birds, plants, and other organisms, which could pose a significant challenge to global ecosystem management. Although other factors such as urbanisation, deforestation, monoculture, and industrialisation may have contributed to the decline in insect species, the extensive application of agro-chemicals appears to cause the most serious threat. Therefore, the development of sustainable and environmentally friendly management strategies is critical for mitigating insect species’ decline.
[Quandahor, P. et al. (2024) Effects of agricultural pesticides on decline in insect species and individual numbers, Environments. Available at: https://www.mdpi.com/2076-3298/11/8/182.]
Tillage practices and the use of pesticide seed treatments (PST) both have the potential to influence epigeal arthropod communities and the ecosystem services they provide, yet few studies have examined both factors in conjunction. A three-year field study (2017–2019) was conducted to assess the independent and interactive effects of tillage and pesticide seed treatments on epigeal arthropod communities and weed seed predation in a long-term row crop tillage intensity experiment located in southeastern New Hampshire, USA. Throughout the study, maize and soybean were planted in rotation with and without pesticide seed treatments (seed coatings containing a mixture of systemic and contact fungicides and neonicotinoid insecticides) under three tillage systems (full-, strip-, and no-till) in a randomized complete block design with four replications. Epigeal arthropod communities were sampled with pitfall traps from September to October 2018–2019 and weed seed predation was assessed over the same period each year from 2017–2019. A total of 1669 individual arthropods, representing 47 taxonomic groups, were observed over the course of the study. In 2018, epigeal arthropod communities differed based only on pesticide seed treatment. The opposite response was observed in 2019, as epigeal arthropod communities differed based only on tillage. Activity densities of Pterostichus melanarius (Illiger) were higher in the strip-till compared to full-till treatment in 2018. Annual levels of post-dispersal weed seed predation by invertebrates (% total seeds removed) varied based on tillage treatment in 2017 and 2019, but not in 2018, and ranged from as low as 6.1 % to as much as 27.2 % depending on year and treatment. These data provide evidence that both pesticide seed treatments and tillage systems can influence the communities of epigeal arthropods that inhabit annual row crop agroecosystems relatively late in the growing season, when the majority of pesticide residues have likely dissipated, and that the weed seed predation services provided by members of this community can be strongly negatively impacted by intensive tillage.
[Ativor, I., Warren, N. and Smith, R. (2024) Effects of tillage intensity and pesticide treated seeds on epigeal arthropod communities and weed seed predation in a maize-soybean rotation, Agriculture, Ecosystems & Environment. Available at: https://www.sciencedirect.com/science/article/abs/pii/S0167880924004560. ]
Increasing agriculture and pesticide use have led to declines in insect populations and biodiversity worldwide. In addition to insect diversity, it is also important to consider insect abundance, due to the importance of insects as food for species at higher trophic levels such as bats. We monitored spatiotemporal variation in abundance of nocturnal flying insects over meadows, a common open landscape structure in central Europe, and correlated it with bat feeding activity. Our most important result was that insect abundance was almost always extremely low. This was true regardless of management intensity of the different meadows monitored. We also found no correlation of insect abundance or the presence of insect swarms with bat feeding activity. This suggests that insect abundance over meadows was too low and insect swarms too rare for bats to risk expending energy to search for them. Meadows appeared to be poor habitat for nocturnal flying insects, and of low value as a foraging habitat for bats. Our study highlights the importance of long-term monitoring of insect abundance, especially at high temporal scales to identify and protect foraging habitats. This will become increasingly important given the rapid decline of insects.
[Dietzer, M. et al. (2024) High temporal resolution data reveal low bat and insect activity over managed meadows in Central Europe, Scientific Reports. Available at: https://www.nature.com/articles/s41598-024-57915-0. ]
Mounting evidence shows overall insect abundances are in decline globally. Habitat loss, climate change, and pesticides have all been implicated, but their relative effects have never been evaluated in a comprehensive large-scale study. We harmonized 17 years of land use, climate, multiple classes of pesticides, and butterfly survey data across 81 counties in five states in the US Midwest. We find community-wide declines in total butterfly abundance and species richness to be most strongly associated with insecticides in general, and for butterfly species richness the use of neonicotinoid-treated seeds in particular. This included the abundance of the migratory monarch (Danaus plexippus), whose decline is the focus of intensive debate and public concern. Insect declines cannot be understood without comprehensive data on all putative drivers, and the 2015 cessation of neonicotinoid data releases in the US will impede future research.
[Deynze, B.V. et al. (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. Available at: https://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0304319. ]
Despite the major role that insect pollinators play in crop production, agricultural intensification drives them into decline. Various conservation measures have been developed to mitigate the negative effects of agriculture on insect pollinators.
In a novel comparison of the efficacy of three conservation measures on honeybee colony growth, we monitored experimental honeybee colonies in 16 landscapes that comprised orthogonal gradients of organic agriculture, annual flower strips and perennial semi-natural habitats. Using structural equation modelling, we assessed the effects of conservation measures on the prevalence of 11 parasites, Varroa destructor loads and their collective impact on colony growth.
Increasing area coverage of perennial semi-natural habitat related to higher V. destructor load and indirectly to lower colony growth.
Increasing area of annual flower strips was associated with lower V. destructor load and indirectly with higher colony growth.
Increasing area of organic farming related to lower parasite richness and also directly to improved colony growth.
Synthesis and applications: Landscape features can affect pollinators directly through the provision of food resources and indirectly through modulation of parasite prevalence. To promote honeybee colony health in agro-ecosystems, our results suggest that organic agriculture and annual flower strips should be prioritized conservation measures. Landscape management should consider the merits and demerits of different measures to sustain healthy populations of pollinators in agro-ecosystems.
[Pluta, P. et al. (2024) Organic farming and annual flower strips reduce parasite prevalence in honeybees and boost colony growth in agricultural landscapes, Journal of Applied Ecology. Available at: https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2664.14723. ]
Insect biomass is declining globally, likely driven by climate change and pesticide use, yet systematic studies on the effects of various chemicals remain limited. In this work, we used a chemical library of 1024 molecules—covering insecticides, herbicides, fungicides, and plant growth inhibitors—to assess the impact of sublethal pesticide doses on insects. In Drosophila melanogaster, 57% of chemicals affected larval behavior, and a higher proportion compromised long-term survivability. Exposure to sublethal doses also induced widespread changes in the phosphoproteome and changes in development and reproduction. The negative effects of agrochemicals were amplified when the temperature was increased. We observed similar behavioral changes across multiple insect species, including mosquitoes and butterflies. These findings suggest that widespread sublethal pesticide exposure can alter insect behavior and physiology, threatening long-term population survival.
[Gandara, L. et al. (2024) Pervasive sublethal effects of agrochemicals on insects at environmentally relevant concentrations, Science. Available at: https://www.science.org/doi/10.1126/science.ado0251. ]
Ecological risk assessments (ERAs) are crucial when developing national strategies to manage adverse effects from pesticide exposure to natural populations. Yet, estimating risk with surrogate species in controlled laboratory studies jeopardizes the ERA process because natural populations exhibit intraspecific variation within and across species. Here, we investigate the extent to which the ERA process underestimates the risk from pesticides on different species by conducting a meta-analysis of all records in the ECOTOX Knowledgebase for honey bees and wild bees exposed to neonicotinoids. We found the knowledgebase is largely populated by acute lethality data on the Western honey bee and exhibits within and across species variation in LD50 up to 6 orders of magnitude from neonicotinoid exposure. We challenge the reliability of surrogate species as predictors when extrapolating pesticide toxicity data to wild pollinators and recommend solutions to address the (a)biotic interactions occurring in nature that make such extrapolations unreliable in the ERA process.
[Shahmohamadloo, R., Guzman, L. and Tissier, M. (2024) Risk assessments underestimate threat of pesticides to wild bees, Conservation Letters. Available at: https://conbio.onlinelibrary.wiley.com/doi/full/10.1111/conl.13022. ]
Bees carry out vital ecosystem services by pollinating both wild and economically important crop plants. However, while performing this function, bee pollinators may encounter potentially harmful xenobiotics in the environment such as pesticides (fungicides, herbicides and insecticides). Understanding the key factors that influence the toxicological outcomes of bee exposure to these chemicals, in isolation or combination, is essential to safeguard their health and the ecosystem services they provide. In this regard, recent work using toxicogenomic and phylogenetic approaches has begun to identify, at the molecular level, key determinants of pesticide sensitivity in bee pollinators. These include detoxification systems that convert pesticides to less toxic forms and key residues in insecticide target-sites that underlie species-specific insecticide selectivity. Here we review this emerging body of research and summarise the state of knowledge of the molecular determinants of pesticide sensitivity in bee pollinators. We identify gaps in our knowledge for future research and examine how an understanding of the genetic basis of bee sensitivity to pesticides can be leveraged to, a) predict and avoid negative bee-pesticide interactions and facilitate the future development of pest-selective bee-safe insecticides, and b) inform traditional effect assessment approaches in bee pesticide risk assessment and address issues of ecotoxicological concern.
[Bass, C. et al (2024) The molecular determinants of pesticide sensitivity in bee pollinators, Science of The Total Environment. Available at: https://www.sciencedirect.com/science/article/pii/S0048969724003097.]
Biodiversity plays a fundamental role in enhancing agricultural resilience and sustaining food production by supporting critical ecosystem services. A diverse array of species within agroecosystems, from crops and livestock to soil organisms and pollinators, contributes to the stability, productivity, and adaptability of farming systems. This biodiversity-driven resilience is essential for mitigating the impacts of climate change, pests, diseases, and resource scarcity, which pose significant threats to global food security. Agricultural systems rich in biodiversity benefit from improved soil fertility, enhanced pollination, natural pest control, and water regulation, all of which reduce dependence on external inputs such as chemical fertilizers and pesticides. Moreover, maintaining genetic diversity within crops and livestock strengthens resilience against environmental stressors and promotes long-term sustainability. However, modern intensive agricultural practices, including monocropping and the overuse of agrochemicals, have resulted in significant biodiversity loss, compromising ecosystem health. This article explores the role of biodiversity in agricultural resilience, examines the threats posed by conventional farming practices, and discusses strategies for integrating biodiversity into agricultural systems to protect ecosystem services. By fostering biodiversity, farmers and policymakers can enhance the sustainability and resilience of agricultural landscapes, contributing to global food security in a changing climate.
[Christianah, D. and Folarin, I. (2024) The Role of Biodiversity in Agricultural Resilience: Protecting Ecosystem Services for Sustainable Food Production, International Journal of Research Publication and Reviews. Available at: https://www.researchgate.net/publication/384848907_The_Role_of_Biodiversity_in_Agricultural_Resilience_Pr]
In North America, approximately 21 % (739 species) of the total wild bee diversity is known to be associated with crops, with bee species varying in the extent of this association. While current evaluations of pesticide effects on bees primarily focus on a limited subset of species, a new focus is needed to ensure comprehensive protection of all wild bees in agricultural contexts. This study introduces a novel approach to characterize and compare the relative potential pesticide risk for wild bee species of their association with crops. Using intrinsic bee vulnerability traits and extrinsic factors like crop toxic loads and association strength, we calculated Bee-Crop Risk Scores for 594 wild bee species, identifying those experiencing the highest potential risk from pesticide exposure in North American agroecosystems. We discuss the influence of intrinsic and extrinsic factors on the relative potential risk calculated and outline avenues for refining our approach. As most species facing the highest potential risk from pesticide exposure across North America are ground-nesters, our study suggests that species (e.g., Osmia spp., Megachile spp.) commonly proposed as models for pesticide risk assessments may not accurately represent risk for those bee species facing the highest potential risk in agricultural contexts.
[Chan, D. and Rondeau, S. (2024) Understanding and comparing relative pesticide risk among North American wild bees from their association with agriculture, Science of The Total Environment. Available at: https://www.sciencedirect.com/science/article/pii/S0048969724055281.]
Temperature increases and land-use changes induce altered annual activity periods of arthropods. However, sufficiently resolved long-term data sets (> 100 years) are mostly missing. We use a data set of longhorn beetle records (71 species) collected in Luxembourg 1864–2014. Increase of annual temperatures was significantly correlated with an earlier annual appearance. Forty-four species present before and after 1980 appeared on average 8.2 days earlier in the year in the more recent period. Since 1950, the estimated shift was 0.26 days per year. Increase of temperature in spring (March–June) preponed the first appearance of beetles by on average 9.6 days per 1 °C. We found significant changes in the composition of beetle communities, with a net gain in species richness during the last 40 years. Eleven species recorded only after 1997 were characterized by comparatively early annual appearance. Smaller beetles tended to appear earlier in the year in comparison to large-bodied species. Shifts in phenology did not correlate with species Red List status. As also demonstrated by our data, climate change in general affects insect phenologies and changes species composition. However, land-use change has taken place in parallel with climate change. Both aspects of global change are influencing the changes in longhorn beetle occurrences in Luxemburg in their combination. This might be most clearly reflected in the strong decrease of species with continental climate niches dwelling in old-growth deciduous forests that apparently are threatened by the loss of these habitats and increasing spring temperatures.
[Vitali, F., Habel, J.C., Ulrich, W. et al. Global change drives phenological and spatial shifts in Central European longhorn beetles (Coleoptera, Cerambycidae) during the past 150 years. Oecologia 202, 577–587 (2023). https://doi.org/10.1007/s00442-023-05417-7]
Declining bee populations diminish pollination services, damaging plant and agricultural biodiversity. One of the causes of this decline is the use of pesticides. Pesticides with glyphosate as the main active ingredient are among the most used pesticides worldwide, being the most used in Brazil. This study determined the 24 and 48 h LD50 (median lethal dose) of the herbicide’s glyphosate-based formulation by ingestion, identified sublethal doses, and investigated its effects on the locomotion and behavior of Tetragonisca angustula workers. The LD50 found indicates that a glyphosate-based formulation is highly toxic to T. angustula. The doses applied, including concentrations found in nature, caused death, motor changes (decreased speed and tremors), excessive self-cleaning, and disorientation (return to light and stop). Although we did not test for pollination effects, we can infer from our results that this formulation can negatively affect the pollination activity of T. angustula. Evaluation of the toxicity and sublethal effects of pesticides on bees contributes to a better understanding of their harmful effects on hives and allows for the development of strategies to reduce these impacts.
[Prado, I.S., da Rocha, A.A., Silva, L.A. and Gonzalez, V.C., 2023. Ecotoxicology, 32(4), pp.513-524.]
Conservation agriculture practices such as eliminating tillage and planting high residue cover crops are becoming increasingly important in field crop systems in the US Mid-Atlantic. However, these practices have sometimes been associated with an increase in moderate to severe damage to field crops by slugs. Conserving natural enemy populations is a desirable way to manage slug infestations because remedial control measures are limited. Here, we tested the effects of conservation practices, weather, and natural enemies on slug activity-density measured by tile traps placed among 41 corn and soybean fields during the spring of 2018 and 2019 in the Northern Shenandoah Valley, Virginia, USA. We found that a positive effect of cover crops on slug activity-density was reduced by tillage and that slug activity-density declined with increasing ground beetle activity-density. Slug activity-density also declined with decreasing rainfall and increasing average temperature. Weather was the only significant predictor of ground beetle activity-density, which was reduced in sites and weeks that were relatively hot and dry or that were cool and wet. However, we also found a marginally significant negative effect of pre-plant insecticides on ground beetles. We suggest that the observed interacting effects of cover crops and tillage reflect favorable conditions for slugs provided by increased small grain crop residue that can be mitigated to some extent by even low levels of tillage. More broadly, our study suggests that implementation of practices known to promote recruitment of ground beetles in crop fields can improve natural suppression of slugs in corn and soybean that are being increasingly cultivated according to conservation agriculture practices.
[Thabu Mugala, Kirsten Brichler, Bobby Clark, Gareth S Powell, Sally Taylor, Michael S Crossley, Ground beetles suppress slugs in corn and soybean under conservation agriculture, Environmental Entomology, Volume 52, Issue 4, August 2023, Pages 574–582, https://doi.org/10.1093/ee/nvad047]
The continuing decline in the diversity and biomass of insects and other arthropods has caused great concern not only among scientists, but also among society, policymakers and stakeholders. A major reason for this is that many ecosystem services depend on diverse insect communities. Despite numerous studies on the dynamics of insect communities, their causes are still not fully understood. Rather than focusing on additional evidence of population declines, this special feature addresses the causes and consequences of population and diversity trends, aiming at a better mechanistic understanding of the observed dynamics.
[Gossner Martin M., Menzel Florian and Simons Nadja K. (2023) Less overall, but more of the same: drivers of insect population trends lead to community homogenization, Biol. Lett.1920230007
http://doi.org/10.1098/rsbl.2023.0007]
Even though honey bees in the field are routinely exposed to a complex mixture of many different agrochemicals, few studies have surveyed toxic effects of pesticide mixtures on bees. To elucidate the interactive actions of pesticides on crop pollinators, we determined the individual and joint toxicities of thiamethoxam (THI) and other seven pesticides [dimethoate (DIM), methomyl (MET), zeta-cypermethrin (ZCY), cyfluthrin (CYF), permethrin (PER), esfenvalerate (ESF) and tetraconazole (TET)] to honey bees (Aplis mellifera) with feeding toxicity test. Results from the 7-days toxicity test implied that THI elicited the highest toxicity with a LC50 data of 0.25 (0.20–0.29) μg mL−1, followed by MET and DIM with LC50 data of 4.19 (3.58–4.88) and 5.30 (4.65–6.03) μg mL−1, respectively. By comparison, pyrethroids and TET possessed relatively low toxicities with their LC50 data from the range of 33.78 (29.12–38.39) to 1125 (922.4–1,442) μg mL−1. Among 98 evaluated THI-containing binary to octonary mixtures, 29.59% of combinations exhibited synergistic effects. In contrast, 18.37% of combinations exhibited antagonistic effects on A. mellifera. Moreover, 54.8% pesticide combinations incorporating THI and TET displayed synergistic toxicities to the insects. Our findings emphasized that the coexistence of several pesticides might induce enhanced toxicity to honey bees. Overall, our results afforded worthful toxicological information on the combined actions of neonicotinoids and current-use pesticides on honey bees, which could accelerate farther comprehend on the possible detriments of other pesticide mixtures in agro-environment.
[Li, W. et al. (2023) Mixture effects of thiamethoxam and seven pesticides with different modes of action on honey bees (Aplis mellifera), Scientific Reports. Available at: https://www.nature.com/articles/s41598-023-29837-w#ref-CR30. ]
Piperonyl butoxide (PBO) is a popular insecticide synergist present in thousands of commercial, agricultural, and household products. PBO inhibits cytochrome P450 activity, impairing the ability of insects to detoxify insecticides. PBO was recently discovered to also inhibit Sonic hedgehog signaling, a pathway required for embryonic development, and rodent studies have demonstrated the potential for in utero PBO exposure to cause structural malformations of the brain, face, and limbs, or more subtle neurodevelopmental abnormalities. The current understanding of the pharmacokinetics of PBO in mice is limited, particularly with respect to dosing paradigms associated with developmental toxicity. To establish a pharmacokinetic (PK) model for oral exposure, PBO was administered to female C57BL/6J mice acutely by oral gavage (22–1800 mg/kg) or via diet (0.09 % PBO in chow). Serum and adipose samples were collected, and PBO concentrations were determined by HPLC-MS/MS. The serum concentrations of PBO were best fit by a linear one-compartment model. PBO concentrations in visceral adipose tissue greatly exceeded those in serum. PBO concentrations in both serum and adipose tissue decreased quickly after cessation of dietary exposure. The elimination half-life of PBO in the mouse after gavage dosing was 6.5 h (90 % CI 4.7–9.5 h), and systemic oral clearance was 83.3 ± 20.5 mL/h. The bioavailability of PBO in chow was 41 % that of PBO delivered in olive oil by gavage. Establishment of this PK model provides a foundation for relating PBO concentrations that cause developmental toxicity in the rodent models to Sonic hedgehog signaling pathway inhibition.
[Jenkins, A. et al. (2023) Pharmacokinetic analysis of acute and dietary exposure to piperonyl butoxide in the mouse, Toxicology Reports. Available at: https://www.sciencedirect.com/science/article/pii/S2214750023001099. ]
The widespread use of glyphosate-based formulations to eliminate unwanted vegetation has increased concerns regarding their effects on non-target organisms, such as honey bees and their gut microbial communities. These effects have been associated with both glyphosate and co-formulants, but it is still unknown whether they translate to other bee species. In this study, we tested whether glyphosate, pure or in herbicide formulation, can affect the gut microbiota and survival rates of the eastern bumble bee, Bombus impatiens. We performed mark-recapture experiments with bumble bee workers from four different commercial colonies, which were exposed to field relevant concentrations of glyphosate or a glyphosate-based formulation (0.01 mM to 1 mM). After a 5-day period of exposure, we returned the bees to their original colonies, and they were sampled at days 0, 3 and 7 post-exposure to investigate changes in microbial community and microbiota resilience by 16S rRNA amplicon sequencing and quantitative PCR. We found that exposure to glyphosate, pure or in herbicide formulation, reduced the relative abundance of a beneficial bee gut bacterium, Snodgrassella, in bees from two of four colonies when compared to control bees at day 0 post-exposure, but this reduction became non-significant at days 3 and 7 post-exposure, suggesting microbiota resilience. We did not find significant changes in total bacteria between control and exposed bees. Moreover, we observed an overall trend in decreased survival rates in bumble bees exposed to 1 mM herbicide formulation during the 7-day post-exposure period, suggesting a potential negative effect of this formulation on bumble bees.
[Motta, E.V. and Moran, N.A., 2023. Science of The Total Environment, 872, p.162102.]
Several previous studies have investigated changes in insect biodiversity, with some highlighting declines and others showing turnover in species composition without net declines. Although research has shown that biodiversity changes are driven primarily by land-use change and increasingly by climate change, the potential for interaction between these drivers and insect biodiversity on the global scale remains unclear. Here we show that the interaction between indices of historical climate warming and intensive agricultural land use is associated with reductions of almost 50% in the abundance and 27% in the number of species within insect assemblages relative to those in less-disturbed habitats with lower rates of historical climate warming. These patterns are particularly evident in the tropical realm, whereas some positive responses of biodiversity to climate change occur in non-tropical regions in natural habitats. A high availability of nearby natural habitat often mitigates reductions in insect abundance and richness associated with agricultural land use and substantial climate warming but only in low-intensity agricultural systems. In such systems, in which high levels (75% cover) of natural habitat are available, abundance and richness were reduced by 7% and 5%, respectively, compared with reductions of 63% and 61% in places where less natural habitat is present (25% cover). Our results show that insect biodiversity will probably benefit from mitigating climate change, preserving natural habitat within landscapes and reducing the intensity of agriculture.
[Outhwaite, C.L., McCann, P. and Newbold, T., Nature, pp.1-6.]
Honeybees use wide-field visual motion information to calculate the distance they have flown from the hive, and this information is communicated to conspecifics during the waggle dance. Seed treatment insecticides, including neonicotinoids and novel insecticides like sulfoxaflor, display detrimental effects on wild and managed bees, even when present at sublethal quantities. These effects include deficits in flight navigation and homing ability, and decreased survival of exposed worker bees. Neonicotinoid insecticides disrupt visual motion detection in the locust, resulting in impaired escape behaviors, but it had not previously been shown whether seed treatment insecticides disrupt wide-field motion detection in the honeybee. Here, we show that sublethal exposure to two commonly used insecticides, imidacloprid (a neonicotinoid) and sulfoxaflor, results in impaired optomotor behavior in the honeybee. This behavioral effect correlates with altered stress and detoxification gene expression in the brain. Exposure to sulfoxaflor led to sparse increases in neuronal apoptosis, localized primarily in the optic lobes, however there was no effect of imidacloprid. We propose that exposure to cholinergic insecticides disrupts the honeybee’s ability to accurately encode wide-field visual motion, resulting in impaired optomotor behaviors. These findings provide a novel explanation for previously described effects of neonicotinoid insecticides on navigation and link these effects to sulfoxaflor for which there is a gap in scientific knowledge.
[Parkinson, R., Fecher, C. and Gray, J. (2022) Chronic exposure to insecticides impairs honeybee optomotor behaviour, Frontiers in Insect Science. Available at: https://www.frontiersin.org/journals/insect-science/articles/10.3389/finsc.2022.936826/full. ]
To study insect decline, an important threat to biodiversity, long-term datasets are needed. Here we present a study of hoverfly (Diptera: Syrphidae) abundance and diversity in a Dutch forest, surrounded by other forests, and analyse the variation in insect numbers over four decades. Between 1982 and 2021, abundance decreased by 80%. Until 1990, abundance showed a strong decrease of 10.9% per year, mainly in nationally rare species with carnivorous larvae exposed to air. From 1990, abundance stabilised, whereas from 2000, a second period of strong decline of 9.0% per year occurred, mainly in very common species. Species richness also declined strongly between 1979 and 2021: the total number of species observed in five monitoring days dropped by 44% over those 43 years. The characteristic set of dry-forest hoverfly species disappeared over four decades. The number of nationally rare species observed at the study site declined from 19 to 9 early on, in a period (1979–1984) that coincided with intense nitrogen input and acidification caused by agriculture in the same region. The more recent decline is likely also caused by factors from outside the forest, as forest management and conditions remained constant. Continued influx of nutrients and pesticides at a regional level, as well as climate change are possible causes of the decline. Research is needed to quantify their relative effects.
[Barendregt, A., Zeegers, T., van Steenis, W. & Jongejans, E. (2022) Forest hoverfly community collapse: Abundance and species richness drop over four decades. Insect Conservation and Diversity, 15(5), 510–521. Available from: https://doi.org/10.1111/icad.12577]
The risk of honey bee (Apis mellifera L.) exposure to pesticide residues while foraging for nectar and pollen is commonly explored in the context of agroecosystems. However, pesticides are also used in urban and suburban areas for vegetation management, vector control, and the management of ornamental plants in public and private landscapes. The extent to which pesticides pose a health risk to honey bees in these settings remains unclear. We addressed this at a landscape scale by conducting pesticide residue screening analyses on 768 nectar and 862 pollen samples collected monthly over 2 years from honey bee colonies located in urban and suburban areas in eight medium to large cities in California, Florida, Michigan, and Texas (USA). A risk assessment was performed using the US Environmental Protection Agency's BeeREX model whenever an oral toxicity value was available for a compound. Chemical analyses detected 17 pesticides in nectar and 60 in pollen samples during the survey. Approximately 73% of all samples contained no detectable pesticide residues. Although the number of detections varied among the sampled regions, fewer pesticides were detected in nectar than in pollen. Per BeeREX, four insecticides showed a potential acute risk to honey bees: imidacloprid, chlorpyrifos, and esfenvalerate in nectar, and deltamethrin in nectar and pollen. In general, exposure of honey bees to pesticides via nectar and pollen collection was low in urban and suburban areas across the United States, and no seasonal or spatial trends were evident. Our data suggest that honey bees are exposed to fewer pesticides in developed areas than in agricultural ones.
[Démares, F.J. et al. (2022) Honey Bee (Apis mellifera) Exposure to Pesticide Residues in Nectar and Pollen in Urban and Suburban Environments from Four Regions of the United States, Environmental Toxicology and Chemistry. Available at: https://setac.onlinelibrary.wiley.com/doi/10.1002/etc.5298. ]
Deltamethrin and piperonyl butoxide two synthetic pyrethroids, when used in a combination it produces synergistic effect. This two insecticide has found to be widely used in the management of mosquito, housefly and other insects to control the various vector born diseases. In this review we assessed the toxic effect of deltamethrin and piperonyl butoxide on beneficial organisms commonly available in the ecosystem. It was found to be toxic to fish, honey bees the prime pollinators of crop plant; earthworm is also susceptible at a lethal concentration for a particular exposure. As far the birds are concerned, they have a less toxic risk in lower concentration of exposure. The alterations obtained in the hematological, biochemical and histopathological studies, further conclude that it can cause environment hazards and toxic to the non-targeted organisms. This investigation gives an insight into the combined toxicological profile of deltamethrin and PBO for better risk assessment and safe use of pyrethroids and their synergist in non-targeted organisms.
[Basak, Mrinmoy and Choudhury, Rejwan Ahmed and Goswami, Priyanka and Dey, Biplab Kumar and Laskar, Moksood Ahmed (2021) A Review on Non-target Toxicity of Deltamethrin and Piperonyl Butoxide: Synergist. Journal of Pharmaceutical Research International, http://scholar.researcherseuropeans.com/id/eprint/323/]
Major declines in insect biomass and diversity, reviewed here, have become obvious and well documented since the end of World War II. Here, we conclude that the spread and intensification of agriculture during the past half century is directly related to these losses. In addition, many areas, including tropical mountains, are suffering serious losses because of climate change as well. Crops currently occupy about 11% of the world’s land surface, with active grazing taking place over an additional 30%. The industrialization of agriculture during the second half of the 20th century involved farming on greatly expanded scales, monoculturing, the application of increasing amounts of pesticides and fertilizers, and the elimination of interspersed hedgerows and other wildlife habitat fragments, all practices that are destructive to insect and other biodiversity in and near the fields. Some of the insects that we are destroying, including pollinators and predators of crop pests, are directly beneficial to the crops. In the tropics generally, natural vegetation is being destroyed rapidly and often replaced with export crops such as oil palm and soybeans. To mitigate the effects of the Sixth Mass Extinction event that we have caused and are experiencing now, the following will be necessary: a stable (and almost certainly lower) human population, sustainable levels of consumption, and social justice that empowers the less wealthy people and nations of the world, where the vast majority of us live, will be necessary.
[Raven, P. and Wagner, D. (2021) Agricultural intensification and climate change are rapidly decreasing insect biodiversity, PNAS. Available at: https://www.pnas.org/doi/abs/10.1073/pnas.2304663120. ]
Critical gaps in understanding how species respond to environmental change limit our capacity to address conservation risks in a timely way. Here, we examine the direct and interactive effects of key global change drivers, including climate change, land use change, and pesticide use, on persistence of 104 odonate species between two time periods (1980–2002 and 2008–2018) within 100 × 100 km quadrats across the USA using phylogenetic mixed models. Non-target effects of pesticides interacted with higher maximum temperatures to contribute to odonate declines. Closely related species responded similarly to global change drivers, indicating a potential role of inherited traits in species’ persistence or decline. Species shifting their range to higher latitudes were more robust to negative impacts of global change drivers generally. Inherited traits related to dispersal abilities and establishment in new places may govern both species’ acclimation to global change and their abilities to expand their range limits, respectively. This work is among the first to assess effects of climate change, land use change, and land use intensification together on Odonata, a significant step that improves understanding of multispecies effects of global change on invertebrates, and further identifies conditions contributing to global insect loss.
[Sirois-Delisle, C. and Kerr, J.T., 2021. ]
Survey data show a large-scale decline in insects. This global decline is often linked to human actions in intensive agricultural areas. To investigate whether this decline has a causal relationship with neonicotinoid insecticides, we performed an outdoor experiment with representative surface water concentrations of the neonicotinoid thiacloprid. We exposed naturally formed aquatic communities to increasing neonicotinoid concentrations and monitored insect emergence during a 3-mo period. We show that increasing neonicotinoid concentrations strongly decreased the abundance and biomass of five major insect orders that together comprised >99% of the 55,574 collected insects as well as the diversity of the most species-rich freshwater family, thus showing a causal relation between insect decline and neonicotinoids.
[Barmentlo, S.H., Schrama, M., De Snoo, G.R., Van Bodegom, P.M., van Nieuwenhuijzen, A. and Vijver, M.G. Proceedings of the National Academy of Sciences, 118(44).]
Semi-natural field borders are frequently used in midwestern U.S. sustainable agriculture. These habitats are meant to help diversify otherwise monocultural landscapes and provision them with ecosystem services, including biological control. Predatory and parasitic arthropods (i.e., potential natural enemies) often flourish in these habitats and may move into crops to help control pests. However, detailed information on the capacity of semi-natural field borders for providing overwintering refuge for these arthropods is poorly understood. In this study, we used soil emergence tents to characterize potential natural enemy communities (i.e., predacious beetles, wasps, spiders, and other arthropods) overwintering in cultivated organic crop fields and adjacent field borders. We found a greater abundance, species richness, and unique community composition of predatory and parasitic arthropods in field borders compared to arable crop fields, which were generally poorly suited as overwintering habitat. Furthermore, potential natural enemies tended to be positively associated with forb cover and negatively associated with grass cover, suggesting that grassy field borders with less forb cover are less well-suited as winter refugia. These results demonstrate that semi-natural habitats like field borders may act as a source for many natural enemies on a year-to-year basis and are important for conserving arthropod diversity in agricultural landscapes.
[Clem, C.S. and Harmon-Threatt, A.N. Journal of Insect Science, 21(3), p.2.]
Seed coating (‘seed treatment’) is the leading delivery method of neonicotinoid insecticides in major crops such as soybean, wheat, cotton and maize. However, this prophylactic use of neonicotinoids is widely discussed from the standpoint of environmental costs. Growing soybean plants from neonicotinoid-coated seeds in field, we demonstrate that soybean aphids (Aphis glycines) survived the treatment, and excreted honeydew containing neonicotinoids. Biochemical analyses demonstrated that honeydew excreted by the soybean aphid contained substantial concentrations of neonicotinoids even one month after sowing of the crop. Consuming this honeydew reduced the longevity of two biological control agents of the soybean aphid, the predatory midge Aphidoletes aphidimyza and the parasitic wasp Aphelinus certus. These results have important environmental and economic implications because honeydew is the main carbohydrate source for many beneficial insects in agricultural landscapes.
[Calvo-Agudo, M., Dregni, J., González-Cabrera, J., Dicke, M., Heimpel, G.E. and Tena, A. Environmental Pollution, 289, p.117813.]
Insecticides are widely used in the Midwestern USA to combat soybean aphids (Aphis glycines), a globally important crop pest. Broad-spectrum foliar insecticides such as chlorpyrifos, lambda-cyhalothrin, and bifenthrin (hereafter, “target insecticides”) are toxic to wildlife in laboratory settings; however, little information exists regarding drift and deposition of these insecticides in fragmented tallgrass prairie grasslands such as those in Minnesota, USA. To address this information gap, target insecticide spray drift and deposition were measured on passive samplers and arthropods in grasslands adjacent to crop fields in Minnesota. Samples were collected at focal soybean field sites immediately following target insecticide application and at reference corn field sites without target insecticide application. Target insecticides were detected 400 m into grasslands at both focal and reference sites. Residues of chlorpyrifos, an insecticide especially toxic to pollinators and birds, were measured above the contact lethal dose (LD50) for honey bees (Apis mellifera) up to 25 m from field edges in adjacent grasslands. Chlorpyrifos residues on arthropods were below the acute oral LD50 for several common farmland bird species but were above the level shown to impair migratory orientation in white-crowed sparrows (Zonotrichia leucophrys). Deposition of target insecticides on passive samplers was inversely associated with distance from field edge and percent canopy cover of grassland vegetation, and positively associated with samplers placed at mid-canopy compared to ground level. Target insecticide deposition on arthropods had an inverse relationship with vertical vegetation density and was positively associated with maximum height of vegetation. Tallgrass prairie with cover ≥25 m from row crop edges may provide wildlife habitat with lower exposure to foliar application insecticides. Prairie management regimes that increase percent canopy cover and density of vegetation may also reduce exposure of wildlife to these insecticides.
[Goebel, K. et al. (2021) Tallgrass prairie wildlife exposure to spray drift from commonly used soybean insecticides in Midwestern USA, Science of The Total Environment. Available at: https://www.sciencedirect.com/science/article/abs/pii/S0048969721068212. ]
Unintentional environmental consequences caused by neonicotinoids reinforce the development of safer alternatives. Sulfoxaflor is considered such an alternative. However, ecological risk of sulfoxaflor remains largely unknown. Here, we investigated the acute and chronic toxicity of sulfoxaflor to a benthic invertebrate, Chironomus kiinensis. Sulfoxaflor showed lower lethality than imidacloprid to midges, with LC50 values of 84.1 (81.5-87.3), 66.3 (34.8-259), and 47.5 (29.5-306) μg/L for 96-h, 10-d, and 23-d exposures, respectively. Conversely, sulfoxaflor significantly inhibited C. kiinensis growth and emergence in chronic exposures when concentrations were above 20 μg/L. Effects on energy production were assessed through in vitro tests using mitochondria isolated from C. kiinensis. Sulfoxaflor disrupted mitochondrial state-3 respiration, meanwhile, adenosine triphosphatase (ATPase) activity and adenosine triphosphate (ATP) production were both inhibited in a dose-dependent manner. The observed mitochondrial dysfunction may be related to the decreased organismal growth and emergence, which could further influence biodiversity. Interestingly, sulfoxaflor uptake in C. kiinensis was detected even after emergence, implying its potential to be transported along food webs and among environmental compartments. This study provides thorough investigations on the toxicity of an emerging neonicotinoid alternative to Chironomidae. Data derived from the current study are useful to inform future ecological risk assessment and benefit problem-solving to the overall agriculture-environment nexus.
[Liu, Peipei & Wu, Fan & Li, Hui-Zhen & You, Jing. (2021). The neonicotinoid alternative sulfoxaflor causes chronic toxicity and impairs mitochondrial energy production in Chironomus kiinensis. Aquatic Toxicology. 235. 105822. 10.1016/j.aquatox.2021.105822. ]
Background
Previous research suggests that fireflies (Coleoptera: Lampyridae) are susceptible to commonly used insecticides. In the United States, there has been a rapid and widespread adoption of neonicotinoid insecticides, predominantly used as seed coatings on large-acreage crops like corn, soy, and cotton. Neonicotinoid insecticides are persistent in soil yet mobile in water, so they have potential to contaminate firefly habitats both in and adjacent to application sites. As a result, fireflies may be at high risk of exposure to neonicotinoids, possibly jeopardizing this already at-risk group of charismatic insects.
Methods
To assess the sensitivity of fireflies to neonicotinoids, we exposed larvae of Photuris versicolor complex and Photinus pyralis to multiple levels of clothianidin-treated soil and monitored feeding behavior, protective soil chamber formation, intoxication, and mortality.
Results
Pt. versicolor and Pn. pyralis larvae exhibited long-term intoxication and mortality at concentrations above 1,000 ng g−1 soil (1 ppm). Under sub-lethal clothianidin exposure, firefly larvae fed less and spent less time in protective soil chambers, two behavioral changes that could decrease larval survival in the wild.
Discussion
Both firefly species demonstrated sub-lethal responses in the lab to clothianidin exposure at field-realistic concentrations, although Pt. versicolor and Pn. pyralis appeared to tolerate higher clothianidin exposure relative to other soil invertebrates and beetle species. While these two firefly species, which are relatively widespread in North America, appear somewhat tolerant of neonicotinoid exposure in a laboratory setting, further work is needed to extend this conclusion to wild populations, especially in rare or declining taxa.
[Pearsons KA, Lower SE, Tooker JF. 2021. Toxicity of clothianidin to common Eastern North American fireflies. PeerJ 9:e12495 https://doi.org/10.7717/peerj.12495]
Acute (96‐h) toxicities of 5 systemic insecticides (chlorantraniliprole, cyantraniliprole, flupyradifurone, flubendiamide, and sulfoxaflor) were tested on larval Chironomus dilutus and compared with the neonicotinoid imidacloprid. Three insecticides were less acutely toxic than imidacloprid (2.5–25 times lower). However, chlorantraniliprole and cyantraniliprole were 1.5 to 1.8 times more toxic to C. dilutus. Thus, these ryanodine receptor agonists could pose a higher risk to aquatic insects than their neonicotinoid predecessors, warranting further studies.
[Erin M. Maloney, Hunter Sykes, Christy Morrissey, Kerry M. Peru, John V. Headley, Karsten Liber, Comparing the Acute Toxicity of Imidacloprid with Alternative Systemic Insecticides in the Aquatic Insect Chironomus dilutus, Environmental Toxicology and Chemistry, Volume 39, Issue 3, 1 March 2020, Pages 587–594, https://doi.org/10.1002/etc.4639]
Systemic insecticides, such as neonicotinoids, are a major contributor towards beneficial insect declines. This has led to bans and restrictions on neonicotinoid use globally, most noticeably in the European Union, where four commonly used neonicotinoids (imidacloprid, thiamethoxam, clothianidin and thiacloprid) are banned from outside agricultural use. While this might seem like a victory for conservation, restrictions on neonicotinoid use will only benefit insect populations if newly emerging insecticides do not have similar negative impacts on beneficial insects. Flupyradifurone and sulfoxaflor are two novel insecticides that have been registered for use globally, including within the European Union. These novel insecticides differ in their chemical class, but share the same mode of action as neonicotinoids, raising the question as to whether they have similar sub-lethal impacts on beneficial insects. Here, we conducted a systematic literature search of the potential sub-lethal impacts of these novel insecticides on beneficial insects, quantifying these effects with a meta-analysis. We demonstrate that both flupyradifurone and sulfoxaflor have significant sub-lethal impacts on beneficial insects at field-realistic levels of exposure. These results confirm that bans on neonicotinoid use will only protect beneficial insects if paired with significant changes to the agrochemical regulatory process. A failure to modify the regulatory process will result in a continued decline of beneficial insects and the ecosystem services on which global food production relies.
[Siviter Harry and Muth Felicity 2020 Do novel insecticides pose a threat to beneficial insects?Proc. R. Soc. B.28720201265 http://doi.org/10.1098/rspb.2020.1265]
The widespread prophylactic usage of neonicotinoid insecticides has a clear impact on non-target organisms. However, the possible effects of long-term exposure on soil-dwelling organisms are still poorly understood especially for social insects with long-living queens. Here, we show that effects of chronic exposure to the neonicotinoid thiamethoxam on black garden ant colonies, Lasius niger, become visible before the second overwintering. Queens and workers differed in the residue-ratio of thiamethoxam to its metabolite clothianidin, suggesting that queens may have a superior detoxification system. Even though thiamethoxam did not affect queen mortality, neonicotinoid-exposed colonies showed a reduced number of workers and larvae indicating a trade-off between detoxification and fertility. Since colony size is a key for fitness, our data suggest long-term impacts of neonicotinoids on these organisms. This should be accounted for in future environmental and ecological risk assessments of neonicotinoid applications to prevent irreparable damages to ecosystems.
[Schläppi, D., Kettler, N., Straub, L., Glauser, G. and Neumann, P., 2020. Communications biology, 3(1), pp.1-9.]
Declining insect population sizes are provoking grave concern around the world as insects play essential roles in food production and ecosystems. Environmental contamination by intense insecticide usage is consistently proposed as a significant contributor, among other threats. Many studies have demonstrated impacts of low doses of insecticides on insect behavior, but have not elucidated links to insecticidal activity at the molecular and cellular levels. Here, the histological, physiological, and behavioral impacts of imidacloprid are investigated in Drosophila melanogaster, an experimental organism exposed to insecticides in the field. We show that oxidative stress is a key factor in the mode of action of this insecticide at low doses. Imidacloprid produces an enduring flux of Ca2+ into neurons and a rapid increase in levels of reactive oxygen species (ROS) in the larval brain. It affects mitochondrial function, energy levels, the lipid environment, and transcriptomic profiles. Use of RNAi to induce ROS production in the brain recapitulates insecticide-induced phenotypes in the metabolic tissues, indicating that a signal from neurons is responsible. Chronic low level exposures in adults lead to mitochondrial dysfunction, severe damage to glial cells, and impaired vision. The potent antioxidant, N-acetylcysteine amide (NACA), reduces the severity of a number of the imidacloprid-induced phenotypes, indicating a causal role for oxidative stress. Given that other insecticides are known to generate oxidative stress, this research has wider implications. The systemic impairment of several key biological functions, including vision, reported here would reduce the resilience of insects facing other environmental challenges.
[Martelli, F., Zhongyuan, Z., Wang, J., Wong, C.O., Karagas, N.E., Roessner, U., Rupasinghe, T., Venkatachalam, K., Perry, T., Bellen, H.J. and Batterham, P., 2020. Proceedings of the National Academy of Sciences, 117(41), pp.25840-25850.]
Recent studies have reported alarming declines in insect populations, but questions persist about the breadth and pattern of such declines. van Klink et al. compiled data from 166 long-term surveys across 1676 globally distributed sites and confirmed declines in terrestrial insects, albeit at lower rates than some other studies have reported (see the Perspective by Dornelas and Daskalova). However, they found that freshwater insect populations have increased overall, perhaps owing to clean water efforts and climate change. Patterns of variation suggest that local-scale drivers are likely responsible for many changes in population trends, providing hope for directed conservation actions.
[van Klink, R. et al. (2020) Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances, Science. Available at: https://www.science.org/doi/10.1126/science.aax9931. ]
The widespread contamination of ecosystems with plant protection products (pesticides in this text) around the world is evident. Pesticide effects on the physiology, activity and diversity of various aquatic and terrestrial non-target organisms is addressed by numerous studies, and many new aspects are also described in a recent Frontiers Research Topic.
We currently observe a deterioration of biodiversity in agricultural landscapes, and the dramatic losses are increasingly discussed by the public. Declines of insect biomass of more than 70% in the last few decades in Germany, the halving of farmland bird populations in Europe and effects on pollinators are widely known. Out of a set of recorded parameters of agricultural intensification (such as field size, fertilizer application, landscape heterogeneity) a unique, pan-European study identified pesticide application as the responsible factor for lower biodiversity of plants, ground beetles, and birds in wheat fields. Recently, a review recognized chemical pollution including pesticides as the second most important driver for the worldwide decline in insect populations. Other drivers were habitat loss and conversion to intensive agriculture, fertilizer inputs, introduced species, and climate change.
[Brühl, C. and Zaller, J. (2019) Biodiversity Decline as a Consequence of an Inappropriate Environmental Risk Assessment of Pesticides, Frontiers in Environmental Science. Available at: https://www.frontiersin.org/journals/environmental-science/articles/10.3389/fenvs.2019.00177/full.]
The global increase in the proportion of land cultivated with pollinator-dependent crops implies increased reliance on pollination services. Yet agricultural practices themselves can profoundly affect pollinator supply and pollination. Extensive monocultures are associated with a limited pollinator supply and reduced pollination, whereas agricultural diversification can enhance both. Therefore, areas where agricultural diversity has increased, or at least been maintained, may better sustain high and more stable productivity of pollinator-dependent crops. Given that >80% of all crops depend, to varying extents, on insect pollination, a global increase in agricultural pollinator dependence over recent decades might have led to a concomitant increase in agricultural diversification. We evaluated whether an increase in the area of pollinator-dependent crops has indeed been associated with an increase in agricultural diversity, measured here as crop diversity, at the global, regional, and country scales for the period 1961–2016. Globally, results show a relatively weak and decelerating rise in agricultural diversity over time that was largely decoupled from the strong and continually increasing trend in agricultural dependency on pollinators. At regional and country levels, there was no consistent relationship between temporal changes in pollinator dependence and crop diversification. Instead, our results show heterogeneous responses in which increasing pollinator dependence for some countries and regions has been associated with either an increase or a decrease in agricultural diversity. Particularly worrisome is a rapid expansion of pollinator-dependent oilseed crops in several countries of the Americas and Asia that has resulted in a decrease in agricultural diversity. In these regions, reliance on pollinators is increasing, yet agricultural practices that undermine pollination services are expanding. Our analysis has thereby identified world regions of particular concern where environmentally damaging practices associated with large-scale, industrial agriculture threaten key ecosystem services that underlie productivity, in addition to other benefits provided by biodiversity.
[Aizen, M. et al. (2019) Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification, Global Change Biology. Available at: https://onlinelibrary.wiley.com/doi/full/10.1111/gcb.14736. ]
The majority of conservation efforts and public attention are focused on large, charismatic mammals and birds such as tigers, pandas and penguins, yet the bulk of animal life, whether measured by biomass, numerical abundance or numbers of species, consists of invertebrates such as insects. Arguably, these innumerable little creatures are far more important for the functioning of ecosystems than their furry or feathered brethren, but until recently we had few long-term data on their population trends. Recent studies from Germany and Puerto Rico suggest that insects may be in a state of catastrophic population collapse: the German data describe a 76% decline in biomass over 26 years, while the Puerto Rican study estimates a decline of between 75% and 98% over 35 years. Corroborative evidence, for example from butterflies in Europe and California (which both show slightly less dramatic reductions in abundance), suggest that these declines are not isolated. The causes are much debated, but almost certainly include habitat loss, chronic exposure to pesticides, and climate change. The consequences are clear; insects are integral to every terrestrial food web, being food for numerous birds, bats, reptiles, amphibians and fish, and performing vital roles such as pollination, pest control and nutrient recycling. Terrestrial and freshwater ecosystems will collapse without insects. These studies are a warning that we may have failed to appreciate the full scale and pace of environmental degradation caused by human activities in the Anthropocene.
[Goulson, D. (2019) The insect apocalypse, and why it matters, Current Biology. Available at: https://www.sciencedirect.com/science/article/pii/S0960982219307961. ]
Biodiversity of insects is threatened worldwide. Here, we present a comprehensive review of 73 historical reports of insect declines from across the globe, and systematically assess the underlying drivers. Our work reveals dramatic rates of decline that may lead to the extinction of 40% of the world's insect species over the next few decades. In terrestrial ecosystems, Lepidoptera, Hymenoptera and dung beetles (Coleoptera) appear to be the taxa most affected, whereas four major aquatic taxa (Odonata, Plecoptera, Trichoptera and Ephemeroptera) have already lost a considerable proportion of species. Affected insect groups not only include specialists that occupy particular ecological niches, but also many common and generalist species. Concurrently, the abundance of a small number of species is increasing; these are all adaptable, generalist species that are occupying the vacant niches left by the ones declining. Among aquatic insects, habitat and dietary generalists, and pollutant-tolerant species are replacing the large biodiversity losses experienced in waters within agricultural and urban settings. The main drivers of species declines appear to be in order of importance: i) habitat loss and conversion to intensive agriculture and urbanisation; ii) pollution, mainly that by synthetic pesticides and fertilisers; iii) biological factors, including pathogens and introduced species; and iv) climate change. The latter factor is particularly important in tropical regions, but only affects a minority of species in colder climes and mountain settings of temperate zones. A rethinking of current agricultural practices, in particular a serious reduction in pesticide usage and its substitution with more sustainable, ecologically-based practices, is urgently needed to slow or reverse current trends, allow the recovery of declining insect populations and safeguard the vital ecosystem services they provide. In addition, effective remediation technologies should be applied to clean polluted waters in both agricultural and urban environments.
[Sánchez-Bayo, F. and Wyckhuys, K. (2019) Worldwide decline of the entomofauna: A review of its drivers, Biological Conservation. Available at: https://www.sciencedirect.com/science/article/abs/pii/S0006320718313636. ]
Neonicotinoids are a group of insecticides commonly used in agriculture. Due to their high water solubility, neonicotinoids can be transported to surface waters and have the potential to be toxic to aquatic life. The present study assessed and compared the acute (48- or 96-h) toxicity of 6 neonicotinoids (acetamiprid, clothianidin, dinotefuran, imidacloprid, thiacloprid, and thiamethoxam) to 21 laboratory-cultured and field-collected aquatic invertebrates spanning 10 aquatic arthropod orders. Test conditions mimicked species' habitat, with lentic taxa exposed under static conditions, and lotic taxa exposed under recirculating systems. Median lethal concentrations (LC50s) and median effect concentrations (EC50s; immobility) were calculated and used to construct separate lethal- and immobilization-derived species sensitivity distributions for each neonicotinoid, from which 5th percentile hazard concentrations (HC5s) were calculated. The results showed that the most sensitive invertebrates were insects from the orders Ephemeroptera (Neocloeon triangulifer) and Diptera (Chironomus dilutus), whereas cladocerans (Daphnia magna, Ceriodaphnia dubia) were the least sensitive. The HC5s were compared with neonicotinoid environmental concentrations from Ontario (Canada) monitoring studies. For all neonicotinoids except imidacloprid, the resulting hazard quotients indicated little to no hazard in terms of acute toxicity to aquatic communities in Ontario freshwater streams. For the neonicotinoid imidacloprid, a moderate hazard was found when only invertebrate immobilization, and not lethality, data were considered.
[Raby, M., Nowierski, M., Perlov, D., Zhao, X., Hao, C., Poirier, D. G., & Sibley, P. K. (2018). Acute toxicity of 6 neonicotinoid insecticides to freshwater invertebrates. Environmental toxicology and chemistry, 37(5), 1430–1445. https://doi.org/10.1002/etc.4088]
Agricultural intensification is a leading cause of global biodiversity loss, which can reduce the provisioning of ecosystem services in managed ecosystems. Organic farming and plant diversification are farm management schemes that may mitigate potential ecological harm by increasing species richness and boosting related ecosystem services to agroecosystems. What remains unclear is the extent to which farm management schemes affect biodiversity components other than species richness, and whether impacts differ across spatial scales and landscape contexts. Using a global metadataset, we quantified the effects of organic farming and plant diversification on abundance, local diversity (communities within fields), and regional diversity (communities across fields) of arthropod pollinators, predators, herbivores, and detritivores. Both organic farming and higher in-field plant diversity enhanced arthropod abundance, particularly for rare taxa. This resulted in increased richness but decreased evenness. While these responses were stronger at local relative to regional scales, richness and abundance increased at both scales, and richness on farms embedded in complex relative to simple landscapes. Overall, both organic farming and in-field plant diversification exerted the strongest effects on pollinators and predators, suggesting these management schemes can facilitate ecosystem service providers without augmenting herbivore (pest) populations. Our results suggest that organic farming and plant diversification promote diverse arthropod metacommunities that may provide temporal and spatial stability of ecosystem service provisioning. Conserving diverse plant and arthropod communities in farming systems therefore requires sustainable practices that operate both within fields and across landscapes.
[Lichtenberg EM, Kennedy CM, Kremen C, et al. A global synthesis of the effects of diversified farming systems on arthropod diversity within fields and across agricultural landscapes. Glob Change Biol. 2017; 23: 4946–4957. https://doi.org/10.1111/gcb.13714]
We investigated relationships among insecticides and aquatic invertebrate communities in 22 streams of two soy production regions of the Argentine Pampas over three growing seasons. Chlorpyrifos, endosulfan, cypermethrin, and lambda-cyhalothrin were the insecticides most frequently detected in stream sediments. The Species at Risk (SPEAR) pesticide bioassessment index (SPEARpesticides) was adapted and applied to evaluate relationships between sediment insecticide toxic units (TUs) and invertebrate communities associated with both benthic habitats and emergent vegetation habitats. SPEARpesticides was the only response metric that was significantly correlated with total insecticide TU values for all three averaged data sets, consistently showing a trend of decreasing values with increasing TU values (r2 = 0.35 to 0.42, p-value = 0.001 to 0.03). Although pyrethroids were the insecticides that contributed the highest TU values, toxicity calculated based on all insecticides was better at predicting changes in invertebrate communities than toxicity of pyrethroids alone. Crustaceans, particularly the amphipod Hyalella spp., which are relatively sensitive to pesticides, played a large role in the performance of SPEARpesticides, and the relative abundance of all crustaceans also showed a significant decreasing trend with increasing insecticide TUs for two of three data sets (r2 = 0.30 to 0.57, p-value = 0.003 to 0.04) examined. For all data sets, total insecticide TU was the most important variable in explaining variance in the SPEARpesticides index. The present study was the first application of the SPEAR index in South America, and the first one to use it to evaluate effects of pesticides on invertebrate communities associated with aquatic vegetation. Although the SPEAR index was developed in Europe, it performed well in the Argentine Pampas with only minor modifications, and would likely improve in performance as more data are obtained on traits of South American taxa, such as pesticide sensitivity and generation time.
[Hunt, L., Bonetto, C., Marrochi, N., Scalise, A., Fanelli, S., Liess, M., Lydy, M. J., Chiu, M. C., & Resh, V. H. (2017). Species at Risk (SPEAR) index indicates effects of insecticides on stream invertebrate communities in soy production regions of the Argentine Pampas. The Science of the total environment, 580, 699–709. https://doi.org/10.1016/j.scitotenv.2016.12.016]
Neonicotinoid insecticides are commonly-used as seed treatments on flowering crops such as oilseed rape. Their persistence and solubility in water increase the chances of environmental contamination via surface-runoff or drainage into areas adjacent to the crops. However, their uptake and fate into non-target vegetation remains poorly understood. In this study, we analysed samples of foliage collected from neonicotinoid seed-treated oilseed rape plants and also compared the levels of neonicotinoid residues in foliage (range: 1.4–11 ng/g) with the levels found in pollen collected from the same plants (range: 1.4–22 ng/g). We then analysed residue levels in foliage from non-target plants growing in the crop field margins (range: ≤ 0.02–106 ng/g). Finally, in order to assess the possible risk posed by the peak levels of neonicotinoids that we detected in foliage for farmland phytophagous and predatory insects, we compared the maximum concentrations found against the LC50 values reported in the literature for a set of relevant insect species. Our results suggest that neonicotinoid seed-dressings lead to widespread contamination of the foliage of field margin plants with mixtures of neonicotinoid residues, where levels are very variable and discontinuous, but sometimes overlap with lethal concentrations reported for some insect species. Understanding the distribution of pesticides in the environment and their potential effects on biological communities is crucial to properly assess current agricultural management and schemes with biodiversity conservation aims in farmland.
[Botías, C. et al. (2016) Contamination of wild plants near neonicotinoid seed-treated crops, and implications for non-target insects, Science of The Total Environment. Available at: https://www.sciencedirect.com/science/article/abs/pii/S0048969716309950. ]
Wild bee declines have been ascribed in part to neonicotinoid insecticides. While short-term laboratory studies on commercially bred species (principally honeybees and bumblebees) have identified sub-lethal effects, there is no strong evidence linking these insecticides to losses of the majority of wild bee species. We relate 18 years of UK national wild bee distribution data for 62 species to amounts of neonicotinoid use in oilseed rape. Using a multi-species dynamic Bayesian occupancy analysis, we find evidence of increased population extinction rates in response to neonicotinoid seed treatment use on oilseed rape. Species foraging on oilseed rape benefit from the cover of this crop, but were on average three times more negatively affected by exposure to neonicotinoids than non-crop foragers. Our results suggest that sub-lethal effects of neonicotinoids could scale up to cause losses of bee biodiversity. Restrictions on neonicotinoid use may reduce population declines.
[Woodcock, B.A. et al. (2016) Impacts of neonicotinoid use on long-term population changes in wild bees in England, Nature Communications. Available at: https://www.nature.com/articles/ncomms12459. ]
Lethal and sublethal effects of insecticides on target and non-target arthropods are a concern of pest management programs. Cycloneda sanguinea, Orius insidiosus and Chauliognathus flavipes are important biological control agents for aphids, whitefly, lepidopterus eggs, thrips and mites. All three test species were subjected to a toxicity study using the insecticides acephate, bifenthrin, chlorantraniliprole, chlorpyrifos, deltamethrin, imidacloprid, and thiamethoxam. Experiments were done in the lab and field. In the laboratory we evaluated the mortality and sublethal effects of the concentration that killed 20% of the population (LC20) on feeding, repellence and reproduction of the species tested. The lethal effects of these insecticides at the recommended doses was evaluated in the field. Concentration-response bioassays indicated chlorantraniliprole had the lowest toxicity, while chlorpyrifos and acephate were the most toxic. Test species exposed to filter paper surfaces treated with pyrethroids, neonicotinoids and organophosphates were repelled. On the other hand, test species were not repelled from surfaces treated with chlorantraniliprole. Chlorantraniliprole therefore seemed to be the least dangerous insecticide for these three beneficial arthropod test species.
[Fernandes, M. et al. (2016) Lethal and sublethal effects of seven insecticides on three beneficial insects in laboratory assays and field trials, Chemosphere. Available at: https://www.sciencedirect.com/science/article/abs/pii/S0045653516306051. ]
Background
Seed-applied neonicotinoids are widely used in agriculture, yet their effects on non-target species remain incompletely understood. One important group of non-target species is arthropod natural enemies (predators and parasitoids), which contribute considerably to suppression of crop pests. We hypothesized that seed-applied neonicotinoids reduce natural-enemy abundance, but not as strongly as alternative insecticide options such as soil- and foliar-applied pyrethroids. Furthermore we hypothesized that seed-applied neonicotinoids affect natural enemies through a combination of toxin exposure and prey scarcity.
Methods
To test our hypotheses, we compiled datasets comprising observations from randomized field studies in North America and Europe that compared natural-enemy abundance in plots that were planted with seed-applied neonicotinoids to control plots that were either (1) managed without insecticides (20 studies, 56 site-years, 607 observations) or (2) managed with pyrethroid insecticides (eight studies, 15 site-years, 384 observations). Using the effect size Hedge’s d as the response variable, we used meta-regression to estimate the overall effect of seed-applied neonicotinoids on natural-enemy abundance and to test the influence of potential moderating factors.
Results
Seed-applied neonicotinoids reduced the abundance of arthropod natural enemies compared to untreated controls (d = −0.30 ± 0.10 [95% confidence interval]), and as predicted under toxin exposure this effect was stronger for insect than for non-insect taxa (QM = 8.70, df = 1, P = 0.003). Moreover, seed-applied neonicotinoids affected the abundance of arthropod natural enemies similarly to soil- or foliar-applied pyrethroids (d = 0.16 ± 0.42 or −0.02 ± 0.12; with or without one outlying study). Effect sizes were surprisingly consistent across both datasets (I2 = 2.7% for no-insecticide controls; I2 = 0% for pyrethroid controls), suggesting little moderating influence of crop species, neonicotinoid active ingredients, or methodological choices.
Discussion
Our meta-analysis of nearly 1,000 observations from North American and European field studies revealed that seed-applied neonicotinoids reduced the abundance of arthropod natural enemies similarly to broadcast applications of pyrethroid insecticides. These findings suggest that substituting pyrethroids for seed-applied neonicotinoids, or vice versa, will have little net affect on natural enemy abundance. Consistent with previous lab work, our results also suggest that seed-applied neonicotinoids are less toxic to spiders and mites, which can contribute substantially to biological control in many agricultural systems. Finally, our ability to interpret the negative effect of neonicotinoids on natural enemies is constrained by difficulty relating natural-enemy abundance to biological control function; this is an important area for future study.
[Douglas MR, Tooker JF. 2016. Meta-analysis reveals that seed-applied neonicotinoids and pyrethroids have similar negative effects on abundance of arthropod natural enemies. PeerJ 4:e2776 https://doi.org/10.7717/peerj.2776]
Pesticide pollution from agricultural field run-off or spray drift has been documented to impact river ecosystems worldwide. However, there is limited data on short- and long-term effects of repeated pulses of pesticide mixtures on biotic assemblages in natural systems. We used reported pesticide application data as input to a hydrological fate and transport model (Soil and Water Assessment Tool) to simulate spatiotemporal dynamics of pesticides mixtures in streams on a daily time-step. We then applied regression models to explore the relationship between macroinvertebrate communities and pesticide dynamics in the Sacramento River watershed of California during 2002–2013. We found that both maximum and average pesticide toxic units were important in determining impacts on macroinvertebrates, and that the compositions of macroinvertebrates trended toward taxa having higher resilience and resistance to pesticide exposure, based on the Species at Risk pesticide (SPEARpesticides) index. Results indicate that risk-assessment efforts can be improved by considering both short- and long-term effects of pesticide mixtures on macroinvertebrate community composition.
[Chiu, M. C., Hunt, L., & Resh, V. H. (2016). Response of macroinvertebrate communities to temporal dynamics of pesticide mixtures: A case study from the Sacramento River watershed, California. Environmental pollution (Barking, Essex : 1987), 219, 89–98. https://doi.org/10.1016/j.envpol.2016.09.048]
We assessed the state of knowledge regarding the effects of large-scale pollution with neonicotinoid insecticides and fipronil on non-target invertebrate species of terrestrial, freshwater and marine environments. A large section of the assessment is dedicated to the state of knowledge on sublethal effects on honeybees (Apis mellifera) because this important pollinator is the most studied non-target invertebrate species. Lepidoptera (butterflies and moths), Lumbricidae (earthworms), Apoidae sensu lato (bumblebees, solitary bees) and the section "other invertebrates" review available studies on the other terrestrial species. The sections on freshwater and marine species are rather short as little is known so far about the impact of neonicotinoid insecticides and fipronil on the diverse invertebrate fauna of these widely exposed habitats. For terrestrial and aquatic invertebrate species, the known effects of neonicotinoid pesticides and fipronil are described ranging from organismal toxicology and behavioural effects to population-level effects. For earthworms, freshwater and marine species, the relation of findings to regulatory risk assessment is described. Neonicotinoid insecticides exhibit very high toxicity to a wide range of invertebrates, particularly insects, and field-realistic exposure is likely to result in both lethal and a broad range of important sublethal impacts. There is a major knowledge gap regarding impacts on the grand majority of invertebrates, many of which perform essential roles enabling healthy ecosystem functioning. The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols. Despite large knowledge gaps and uncertainties, enough knowledge exists to conclude that existing levels of pollution with neonicotinoids and fipronil resulting from presently authorized uses frequently exceed the lowest observed adverse effect concentrations and are thus likely to have large-scale and wide ranging negative biological and ecological impacts on a wide range of non-target invertebrates in terrestrial, aquatic, marine and benthic habitats.
[Pisa, L. W., Amaral-Rogers, V., Belzunces, L. P., Bonmatin, J. M., Downs, C. A., Goulson, D., Kreutzweiser, D. P., Krupke, C., Liess, M., McField, M., Morrissey, C. A., Noome, D. A., Settele, J., Simon-Delso, N., Stark, J. D., Van der Sluijs, J. P., Van Dyck, H., & Wiemers, M. (2015). Effects of neonicotinoids and fipronil on non-target invertebrates. Environmental science and pollution research international, 22(1), 68–102. https://doi.org/10.1007/s11356-014-3471-x]
Neonicotinoids, broad-spectrum systemic insecticides, are the fastest growing class of insecticides worldwide and are now registered for use on hundreds of field crops in over 120 different countries. The environmental profile of this class of pesticides indicate that they are persistent, have high leaching and runoff potential, and are highly toxic to a wide range of invertebrates. Therefore, neonicotinoids represent a significant risk to surface waters and the diverse aquatic and terrestrial fauna that these ecosystems support. This review synthesizes the current state of knowledge on the reported concentrations of neonicotinoids in surface waters from 29 studies in 9 countries world-wide in tandem with published data on their acute and chronic toxicity to 49 species of aquatic insects and crustaceans spanning 12 invertebrate orders. Strong evidence exists that water-borne neonicotinoid exposures are frequent, long-term and at levels (geometric means=0.13μg/L (averages) and 0.63μg/L (maxima)) which commonly exceed several existing water quality guidelines. Imidacloprid is by far the most widely studied neonicotinoid (66% of the 214 toxicity tests reviewed) with differences in sensitivity among aquatic invertebrate species ranging several orders of magnitude; other neonicotinoids display analogous modes of action and similar toxicities, although comparative data are limited. Of the species evaluated, insects belonging to the orders Ephemeroptera, Trichoptera and Diptera appear to be the most sensitive, while those of Crustacea (although not universally so) are less sensitive. In particular, the standard test species Daphnia magna appears to be very tolerant, with 24-96hour LC50 values exceeding 100,000μg/L (geometric mean>44,000μg/L), which is at least 2-3 orders of magnitude higher than the geometric mean of all other invertebrate species tested. Overall, neonicotinoids can exert adverse effects on survival, growth, emergence, mobility, and behavior of many sensitive aquatic invertebrate taxa at concentrations at or below 1μg/L under acute exposure and 0.1μg/L for chronic exposure. Using probabilistic approaches (species sensitivity distributions), we recommend here that ecological thresholds for neonicotinoid water concentrations need to be below 0.2μg/L (short-term acute) or 0.035μg/L (long-term chronic) to avoid lasting effects on aquatic invertebrate communities. The application of safety factors may still be warranted considering potential issues of slow recovery, additive or synergistic effects and multiple stressors that can occur in the field. Our analysis revealed that 81% (22/27) and 74% (14/19) of global surface water studies reporting maximum and average individual neonicotinoid concentrations respectively, exceeded these thresholds of 0.2 and 0.035μg/L. Therefore, it appears that environmentally relevant concentrations of neonicotinoids in surface waters worldwide are well within the range where both short- and long-term impacts on aquatic invertebrate species are possible over broad spatial scales.
[Morrissey, C. A., Mineau, P., Devries, J. H., Sanchez-Bayo, F., Liess, M., Cavallaro, M. C., & Liber, K. (2015). Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review. Environment international, 74, 291–303. https://doi.org/10.1016/j.envint.2014.10.024]
Neonicotinoids are the most widely used insecticides world-wide, but their fate in the environment remains unclear, as does their potential to influence non-target species and the roles they play in agroecosystems.
We investigated in laboratory and field studies the influence of the neonicotinoid thiamethoxam, applied as a coating to soya bean seeds, on interactions among soya beans, non-target molluscan herbivores and their insect predators.
In the laboratory, the pest slug Deroceras reticulatum was unaffected by thiamethoxam, but transmitted the toxin to predaceous beetles (Chlaenius tricolor), impairing or killing >60%.
In the field, thiamethoxam-based seed treatments depressed activity–density of arthropod predators, thereby relaxing predation of slugs and reducing soya bean densities by 19% and yield by 5%.
Neonicotinoid residue analyses revealed that insecticide concentrations declined through the food chain, but levels in field-collected slugs (up to 500 ng g−1) were still high enough to harm insect predators.
Synthesis and applications. Our findings reveal a previously unconsidered ecological pathway through which neonicotinoid use can unintentionally reduce biological control and crop yield. Trophic transfer of neonicotinoids challenges the notion that seed-applied toxins precisely target herbivorous pests and highlights the need to consider predatory arthropods and soil communities in neonicotinoid risk assessment and stewardship.
[Douglas, M.R., Rohr, J.R. and Tooker, J.F. (2015), EDITOR'S CHOICE: Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soya bean yield. J Appl Ecol, 52: 250-260. https://doi.org/10.1111/1365-2664.12372]
The first neonicotinoid insecticide, imidacloprid, was launched in 1991. Today this class of insecticides comprises at least seven major compounds with a market share of more than 25% of total global insecticide sales. Neonicotinoid insecticides are highly selective agonists of insect nicotinic acetylcholine receptors and provide farmers with invaluable, highly effective tools against some of the world's most destructive crop pests. These include sucking pests such as aphids, whiteflies, and planthoppers, and also some coleopteran, dipteran and lepidopteran species. Although many insect species are still successfully controlled by neonicotinoids, their popularity has imposed a mounting selection pressure for resistance, and in several species resistance has now reached levels that compromise the efficacy of these insecticides. Research to understand the molecular basis of neonicotinoid resistance has revealed both target-site and metabolic mechanisms conferring resistance. For target-site resistance, field-evolved mutations have only been characterized in two aphid species. Metabolic resistance appears much more common, with the enhanced expression of one or more cytochrome P450s frequently reported in resistant strains. Despite the current scale of resistance, neonicotinoids remain a major component of many pest control programmes, and resistance management strategies, based on mode of action rotation, are of crucial importance in preventing resistance becoming more widespread. In this review we summarize the current status of neonicotinoid resistance, the biochemical and molecular mechanisms involved, and the implications for resistance management.
[Bass, Chris & Denholm, Ian & Williamson, Martin & Nauen, Ralf. (2015). The global status of insect resistance to neonicotinoid insecticides. Pesticide Biochemistry and Physiology. 121. 10.1016/j.pestbp.2015.04.004. ]
The toxicological effects of pyrethroids on non-target aquatic insects are mediated by several modes of entry of pyrethroids into aquatic ecosystems, as well as the toxicological characteristics of particular pyrethroids under field conditions. Toxicokinetics, movement across the integument of aquatic insects, and the toxicodynamics of pyrethroids are discussed, and their physiological, symptomatic and ecological effects evaluated. The relationship between pyrethroid toxicity and insecticide uptake is not fully defined. Based on laboratory and field data, it is likely that the susceptibility of aquatic insects (vector and non-vector) is related to biochemical and physiological constraints associated with life in aquatic ecosystems. Understanding factors that influence aquatic insects susceptibility to pyrethroids is critical for the effective and safe use of these compounds in areas adjacent to aquatic environments.
[Antwi, F. B., & Reddy, G. V. (2015). Toxicological effects of pyrethroids on non-target aquatic insects. Environmental toxicology and pharmacology, 40(3), 915–923. https://doi.org/10.1016/j.etap.2015.09.023]
Neonicotinoids are now the most widely used insecticides in the world. They act systemically, travelling through plant tissues and protecting all parts of the crop, and are widely applied as seed dressings. As neurotoxins with high toxicity to most arthropods, they provide effective pest control and have numerous uses in arable farming and horticulture. However, the prophylactic use of broad-spectrum pesticides goes against the long-established principles of integrated pest management (IPM), leading to environmental concerns. It has recently emerged that neonicotinoids can persist and accumulate in soils. They are water soluble and prone to leaching into waterways. Being systemic, they are found in nectar and pollen of treated crops. Reported levels in soils, waterways, field margin plants and floral resources overlap substantially with concentrations that are sufficient to control pests in crops, and commonly exceed the LC50 (the concentration which kills 50% of individuals) for beneficial organisms. Concentrations in nectar and pollen in crops are sufficient to impact substantially on colony reproduction in bumblebees. Although vertebrates are less susceptible than arthropods, consumption of small numbers of dressed seeds offers a route to direct mortality in birds and mammals. Synthesis and applications. Major knowledge gaps remain, but current use of neonicotinoids is likely to be impacting on a broad range of non-target taxa including pollinators and soil and aquatic invertebrates and hence threatens a range of ecosystem services.
[Goulson, D. (2013) An overview of the environmental risks posed by neonicotinoid insecticides, Journal of Applied Ecology. Available at: https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2664.12111. ]
The biodiversity crisis is one of the greatest challenges facing humanity, but our understanding of the drivers remains limited. Thus, after decades of studies and regulation efforts, it remains unknown whether to what degree and at what concentrations modern agricultural pesticides cause regional-scale species losses. We analyzed the effects of pesticides on the regional taxa richness of stream invertebrates in Europe (Germany and France) and Australia (southern Victoria). Pesticides caused statistically significant effects on both the species and family richness in both regions, with losses in taxa up to 42% of the recorded taxonomic pools. Furthermore, the effects in Europe were detected at concentrations that current legislation considers environmentally protective. Thus, the current ecological risk assessment of pesticides falls short of protecting biodiversity, and new approaches linking ecology and ecotoxicology are needed.
[M.A. Beketov, B.J. Kefford, R.B. Schäfer, & M. Liess, Pesticides reduce regional biodiversity of stream invertebrates, Proc. Natl. Acad. Sci. U.S.A. 110 (27) 11039-11043, https://doi.org/10.1073/pnas.1305618110 (2013).]
The development of insecticides requires valid risk assessment procedures to avoid causing harm to beneficial insects and especially to pollinators such as the honeybee Apis mellifera. In addition to testing according to current guidelines designed to detect bee mortality, tests are needed to determine possible sublethal effects interfering with the animal's vitality and behavioral performance. Several methods have been used to detect sublethal effects of different insecticides under laboratory conditions using olfactory conditioning. Furthermore, studies have been conducted on the influence insecticides have on foraging activity and homing ability which require time-consuming visual observation. We tested an experimental design using the radiofrequency identification (RFID) method to monitor the influence of sublethal doses of insecticides on individual honeybee foragers on an automated basis. With electronic readers positioned at the hive entrance and at an artificial food source, we obtained quantifiable data on honeybee foraging behavior. This enabled us to efficiently retrieve detailed information on flight parameters. We compared several groups of bees, fed simultaneously with different dosages of a tested substance. With this experimental approach we monitored the acute effects of sublethal doses of the neonicotinoids imidacloprid (0.15–6 ng/bee) and clothianidin (0.05–2 ng/bee) under field-like circumstances. At field-relevant doses for nectar and pollen no adverse effects were observed for either substance. Both substances led to a significant reduction of foraging activity and to longer foraging flights at doses of ≥0.5 ng/bee (clothianidin) and ≥1.5 ng/bee (imidacloprid) during the first three hours after treatment. This study demonstrates that the RFID-method is an effective way to record short-term alterations in foraging activity after insecticides have been administered once, orally, to individual bees. We contribute further information on the understanding of how honeybees are affected by sublethal doses of insecticides.
[Schneider CW, Tautz J, Grünewald B, Fuchs S (2012) RFID Tracking of Sublethal Effects of Two Neonicotinoid Insecticides on the Foraging Behavior of Apis mellifera. PLOS ONE 7(1): e30023. https://doi.org/10.1371/journal.pone.0030023]
The rove beetle Atheta coriaria (Kraatz) (Coleoptera: Staphylinidae) is a natural enemy (biological control agent) commercially available for control of certain greenhouse insect pests, including fungus gnats, shore flies, and thrips. This study assessed the compatibility of pesticides (insecticides and fungicides) used in greenhouses with A. coriaria adults. Treatments were applied to 473-ml deli squat containers half-filled with a growing medium. We evaluated the effects of the pesticides when releases of A. coriaria adults were performed both before and after application of the designated pesticide solutions. All three of the neonicotinoid-based insecticides (clothianidin, dinotefuran, and thiamethoxam) were directly harmful to A. coriaria adults with ≤3.2 adults recovered (out of 20) among all three treatments across all experiments. In addition, the organophosphate insecticide chlorpyrifos at the low (0.25 fl oz/100 gal) and high (0.50 fl oz/100 gal) label rates; the plant-derived essential oil product (Indoor Pharm) containing soybean and rosemary oil; and the insecticide/miticide chlorfenpyr were directly harmful to A. coriaria adults with recovery rates ≤8.6 (out of 20) among all the treatments. The fungicides (azoxystrobin, fosetyl-aluminum, and mefenoxam) were not directly toxic to A. coriaria adults, with ≥17.7 adults recovered (out of 20) across all experiments. The insecticides (Bacillus thuringiensis subsp. israelensis, flonicamid, Metarhizium anisopliae strain52, and spinosad) and insect growth regulator azadirachtin were also not directly toxic to A. coriaria adults. Furthermore, many of these same treatments did not inhibit the ability of adult A. coriaria to consume fungus gnat (Bradysia sp. nr. coprophila) larvae in a feeding behavior experiment. Although the neonicotinoid-based insecticides were directly harmful to adult A. coriaria, when adults were released 48, 72, or 96 h after application, survival increased dramatically over time. This study has quantitatively demonstrated that certain pesticides (both insecticides and fungicides) are compatible with and can be used along with A. coriaria in systems that use this natural enemy to manage fungus gnat larvae.
[Raymond A. Cloyd, Nicholas R. Timmons, Jessica M. Goebel, Kenneth E. Kemp, Effect of Pesticides on Adult Rove Beetle Atheta coriaria (Coleoptera: Staphylinidae) Survival in Growing Medium, Journal of Economic Entomology, Volume 102, Issue 5, 1 October 2009, Pages 1750–1758, https://doi.org/10.1603/029.102.0504]
Imidacloprid is a neonicotinoid insecticide with neurotoxic action that, as a possible alternative for commonly used organophosphorus pesticides, has gained registration in about 120 countries for use in over 140 agricultural crops. Only few data are available on its toxicity for soil invertebrates. We therefore assessed the effects of imidacloprid on survival, weight gain, feeding rate, total protein content, glutathione S-transferase activity (GST), and digestive gland epithelial thickness in juveniles and adults of the terrestrial isopod Porcellio scaber. After two weeks of feeding on imidacloprid-dosed food, weight gain (NOEC 5 μg/g dry food) and feeding rate (NOEC 10 μg/g) in juveniles, and feeding rate (NOEC < 10 μg/g) and digestive gland epithelial thickness (NOEC < 10 μg/g) in adults were most affected. In juveniles induction of GST activity and increase of total protein content per wet animal weight was detected at 5 μg/g dry food, whereas in adults a reduction of GST was observed at 25 μg/g (NOEC 10 μg/g). An estimate of actual intake rates suggests that imidacloprid affects isopods at similar exposure concentrations as insects. The toxicity of imidacloprid was similar to that of the organophosphorus pesticide diazinon, tested earlier using the same methods [Stanek, K., Drobne, D., Trebse, P., 2006. Linkage of biomarkers along levels of biological complexity in juvenile and adult diazinon fed terrestrial isopod (Porcellio scaber, Isopoda, Crustacea). Chemosphere 64, 1745–1752]. At actual environmental concentrations, diazinon poses a higher risk to P. scaber. Due to its increasing use in crop protection and higher persistence in soil, imidacloprid might however, be potentially more dangerous after long-term application. We conclude that toxicity testing with P. scaber provides relevant, repeatable, reproducible and comparable toxicity data that is useful for the risk assessment of pesticides in the terrestrial environment.
[Drobne, D., Blazic, M., Van Gestel, C. A., Leser, V., Zidar, P., Jemec, A., & Trebse, P. (2008). Toxicity of imidacloprid to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Chemosphere, 71(7), 1326–1334. https://doi.org/10.1016/j.chemosphere.2007.11.042]
Most transgenic corn seed is now treated with systemic neonicotinoid insecticides. To address potential direct nontarget effects of these combined technologies, 16 Carabidae species from 10 genera (Agonum, Amara, Anisodactylus, Bembidion, Chlaenius, Harpalus, Patrobus, Poecilus, Pterostichus, and Scarites) field-collected from corn were directly exposed to Bacillus thuringiensis (Bt) Cry toxin-laden pollens and seed treatments in feeding and defined-dose bioassays. All adults readily fed on field or sweet corn pollens that expressed coleopteran-specific Cry3Bb1 or lepidopteran-targeting Cry1Ab/c, and no significant toxicity was observed. Adult survivorship ranged from 47 d for the predator Pterostichus melanarius (Illiger) to a year for the more omnivorous Scarites quadriceps Chaudoir, feeding solely on pollen containing 30–90 μg Cry3Bb1/g and water. In contrast, commercial doses of neonicotinoid seed treatments (imidacloprid, thiamethoxam, or clothianidin) elicited nearly complete mortality for 18 carabid species in 4-d bioassays containing corn seedlings. Carabid consumption of fungicide-only (fludioxonil plus mefenoxam) seed treatments was generally observed within 1 d, compared with a 2-d latency on neonicotinoid treatments, suggesting an antifeedant effect of the insecticide. In microcosm bioassays containing a corn seedling and five prey, clothianidin seed treatments killed adult western corn rootworm, Diabrotica virgifera virgifera LeConte and S. quadriceps, although the smaller Harpalus pensylvanicus (DeGeer) was more tolerant. We conclude that the neonicotinoid/fungicide seed treatments, and not Cry3Bb1 or CryIAb/c, are a major direct mortality factor for ground beetles. Field studies are needed to determine population and community level effects on Carabidae when these transgenic and seed-treatment technologies are combined.
[Christopher A. Mullin, Michael C. Saunders, Timothy W. Leslie, David J. Biddinger, Shelby J. Fleischer, Toxic and Behavioral Effects to Carabidae of Seed Treatments Used on Cry3Bb1- and Cry1Ab/c-Protected Corn, Environmental Entomology, Volume 34, Issue 6, 1 December 2005, Pages 1626–1636, https://doi.org/10.1603/0046-225X-34.6.1626]