Pollinators
Impact of Pesticides on Pollinators
The science has become increasingly clear that pesticides, either acting individually or synergistically, play a critical role in the ongoing decline of honey bees and wild pollinators. Some pesticides produce sublethal effects in honeybees, which include disruptions in mobility, navigation, and feeding behavior. Decreased foraging activity, along with olfactory learning performance and decreased hive activity has also been observed. Other pollinators, such as the monarch butterfly, are indirectly affected by pesticides through habitat destruction brought on by the proliferation of genetically engineered (GE) crops and mono-crop agriculture. Part of the decline of monarch butterflies stems from the loss of milkweed, a native plant where the butterflies lay their eggs and is their main food source.
- In 2015, researchers found that bumblebees exposed to field levels of neonicotinoids accumulate the toxic pesticides in their brains. Acute and chronic exposure increased neuronal vulnerability to mitochondrial dysfunction.
- Another recent study provided supporting evidence to previous work showing that sublethal doses of imidicloprid, a toxic neonicotinoid insecticide, impairs olfactory learning in exposed honey bee workers. The study found that:
- “Adults that ingested a single imidacloprid dose as low as 0.1 ng/bee had significantly reduced olfactory learning acquisition, which was 1.6-fold higher in control bees.”
- “Bees exposed as larvae to a total dose of 0.24 ng/bee had significantly impaired olfactory learning when tested as adults; control bees exhibited up to 4.8-fold better short-term learning acquisition.”
- In 2014, researches used Radio-Frequency Identification (RFID) tagging technology to examine how the day-to-day foraging patterns of bumblebees were affected when exposed to either a neonicotinoid (imidacloprid) and/or a
pyrethroid (λ-cyhalothrin) independently and in combination over a four-week period. They found that neonicotinoid exposure has both acute and chronic effects on overall foraging activity; the performance of bees exposed to imidacloprid became worse, resulting in chronic behavioral impairment.
Monarch Butterfly on Milkweed. Photo by Lee Ruk. - A recent study on monarchs attributed the disappearance of milkweed plants primarily to the use of GE corn and soybean crops. Scientists also point to the prolific use of herbicides in the Midwest eliminating these plants, and found that 70% of the losses of milkweed between 1995 and 2013 were located in agricultural areas.
[See More Scientific Studies Below]
For more details about the impact of pesticides on pollinators, see Beyond Pesticides’ BEE Protective page.
Economic Cost
In a 2009 study by Gallai et. al., the total economic value of pollinators globally was estimated to be $153 billion per year. Estimates vary for the United States as time moves forward, but regardless of the differing economic figures, the impacts of insecticides used on agriculture to bees and other pollinators are vast. In a 2005 study by David Pimentel, it was estimated that 5% of US honey bee colonies are killed due to pesticide exposure, leading to a $13.3 million annual loss. Honey and wax losses total to about $25.3 million a year. Pimentel speculated that due to the fact that 4-6 million hectares of land are heavily treated with pesticides, beekeepers cannot use what would otherwise be considered suitable apiary land. This yearly loss in potential honey production totals about $27 million. In addition to these losses, many crops fail due to lack of pollination. He estimated that these annual pollination losses caused by pesticides could be as high as $210 million. Pimental’s estimates are conservative, considering they were made before the advent of colony collapse disorder (CCD), and before large-scale pollinator losses began. In 2006, Losey and Vaughan estimated that native pollinators are responsible for $3.07 billion of fruit and vegetable production in the US. Then, in 2012, N.W. Calderone estimated that in 2009, the economic value of crops dependent on pollinators was approximately $15.12 billion for the US.
Litigation & Lawsuits
Beyond Pesticides, concerned citizens, and other environmental organizations filed a civil action suit against EPA in March 2013 for using clothianidin and thiamethoxam, two pesticides classified as neonicotinoids. The lawsuit aims to hold EPA accountable for the violation of Federal Insecticide, Fungicide and Rodenticide Act (FIFRA), the Endangered Species Act (ESA) and the Administrative Procedure Act (APA). EPA has approved the use of these pesticides without notification to the Federal Register, and without a public comment period, which violates FIFRA and the APA.
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| Honeybees. Photo by Paul Rollings. |
In July 2013, several beekeeping organizations filed suit against the U.S. Environmental Protection Agency’s (EPA) to reverse a recent decision to register a new pesticide, sulfoxaflor, which is highly toxic to bees. This chemical is also considered by some scientists to be in the same class as neonicotinoids due to the fact that it has the same mode of action, although industry refuses to consider this claim, In December 2013, environmental and farm groups, including Beyond Pesticides, came together to file a legal brief in support of the nation’s major beekeeping associations’ lawsuit against the EPA. In March 2015, the 9th U.S. Circuit Court of Appeals agreed to hear the case.
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In March 2015, a federal court ruled against the use of neonicotinoid insecticides linked with destruction of bee colonies and other beneficial insects in national wildlife refuges in the Midwest region. The ruling capped a legal campaign to end the planting of genetically engineered (GE) crops and other industrial agricultural practices on national wildlife refuges across the country. In July 2014, FWS decided that it will phase out the use of GE crops to feed wildlife and ban neonicotinoid insecticides from all wildlife refuges nationwide by January 2016. This new policy still allows for case-by-case exceptions.
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What Can You Do?
A necessary first step is to avoid using toxic pesticides in and around your home, and encourage others to do the same. For other helpful tips, see Beyond Pesticides’ webpage on Managing Landscapes with Pollinators in Mind. Concerned residents can find more ways to take action in their community through the BEE Protective webpage.
Scientific Studies:
Sustainable agriculture requires balancing crop yields with the effects of pesticides on non-target organisms, such as bees and other crop pollinators. Field studies demonstrated that agricultural use of neonicotinoid insecticides can negatively affect wild bee species (1,2) leading to restrictions on these compounds (3). However, besides neonicotinoids, field-based evidence of the effects of landscape pesticide exposure on wild bees is lacking. Bees encounter many pesticides in agricultural landscapes (4,5,6,7,8,9) and the effects of this landscape exposure on colony growth and development of any bee species remains unknown. Here we show that the many pesticides found in bumble bee-collected pollen are associated with reduced colony performance during crop bloom, especially in simplified landscapes with intensive agricultural practices. Our results from 316 Bombus terrestris colonies at 106 agricultural sites across eight European countries confirm that the regulatory system fails to sufficiently prevent pesticide-related impacts on non-target organisms, even for a eusocial pollinator species in which colony size may buffer against such impacts (10,11). These findings support the need for postapproval monitoring of both pesticide exposure and effects to confirm that the regulatory process is sufficiently protective in limiting the collateral environmental damage of agricultural pesticide use.
New evidence points to substantial impacts of exposure to pesticide residues in soil for a range of bee taxa that have close regular contact with this substrate. Among others, the risk of exposure is high for bumblebee (Bombus spp.) queens hibernating in agricultural soils. An important question is whether bumblebee queens can detect and avoid pesticide-contaminated soils, or whether they might be attracted to such agrochemical residues. To address this question, we performed a multiple-choice preference experiment in which newly emerged bumblebee (Bombus impatiens) queens were given access to arrays of 36 crates of soil treated with different pesticides in large mesh-covered enclosures. Five of the most commonly encountered pesticides in agricultural soils (boscalid, chlorantraniliprole, clothianidin, cyantraniliprole, difenoconazole) were selected for testing at two contamination levels (lower or higher), based on field-realistic exposure estimates. Bumblebee queens consistently avoided hibernating in pesticide-free soil at both contamination levels, while showing no avoidance for any pesticide-treated soil types. At the lower contamination level, queens selected the pesticide-free soil 1.3 to 2.4-fold less frequently on average than any of the spiked soils, while none of the queens from the higher contamination group selected pesticide-free soil. This apparent preference for pesticide-contaminated soils increases the likelihood of exposure to and potential hazard from pesticide residues in soil for bumblebee queens during hibernation, a critical and highly vulnerable period of their annual life cycle.
[Rondeau, S. and Raine, N. (2024) Bumblebee (Bombus impatiens) queens prefer pesticide-contaminated soils when selecting underground hibernation sites, The Science of the Total Environment. Available at: https://pubmed.ncbi.nlm.nih.gov/39332727/. ]
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.]
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. ]
Agrochemical exposure is a major contributor to ecological declines worldwide, including the loss of crucial pollinator species. In addition to direct toxicity, field-relevant doses of pesticides can increase species’ vulnerabilities to other stressors, including parasites. Experimental field demonstrations of potential interactive effects of pesticides and additional stressors are rare, as are tests of mechanisms via which pollinators tolerate pesticides. Here, we controlled honey bee colony exposure to field-relevant concentrations of 2 neonicotinoid insecticides (clothianidin and thiamethoxam) in pollen and simultaneously manipulated intracolony genetic heterogeneity. We showed that exposure increased rates of Varroa destructor (Anderson and Trueman) parasitism and that while increased genetic heterogeneity overall improved survivability, it did not reduce the negative effect size of neonicotinoid exposure. This study is, to our knowledge, the first experimental field demonstration of how neonicotinoid exposure can increase V. destructor populations in honey bees and also demonstrates that colony genetic diversity cannot mitigate the effects of neonicotinoid pesticides.
[Bartlett, L.J. et al. (2024) Neonicotinoid exposure increases Varroa destructor (Mesostigmata: Varroidae) mite parasitism severity in honey bee colonies and is not mitigated by increased colony genetic diversity, Journal of Insect Science. Available at: https://academic.oup.com/jinsectscience/article/24/3/20/7683866.]
Honey bees are constantly threatened due to the wide use of pesticides. This study presents the effects of deltamethrin on the mortality, olfactory learning, and memory formation of the native Saudi bee Apis mellifera jemenitica. Topical and oral application of realistic field and serial dilutions of deltamethrin (250, 125, 62.5, and 25 ppm) caused significant mortality at 4, 12, 24, and 48 h posttreatment. Bee mortality increased with the increasing concentration of insecticide at all tested posttreatment times. Highest mortality was observed at 24 h and 48 h after both exposure routes. Food consumption gradually decreased with increasing concentration of deltamethrin during oral exposure. The LC50 of deltamethrin was determined at 12, 24, and 48 h for topical (86.28 ppm, 36.16 ppm, and 29.19 ppm, respectively) and oral (35.77 ppm, 32.53 ppm, and 30.78 ppm, respectively) exposure. Oral exposure led to significantly higher bee mortality than topical exposure of deltamethrin at 4 h and 12 h, but both exposure routes were equally toxic to bees at 24 h and 48 h. The sublethal concentrations (LC10, LC20, and LC30) of deltamethrin significantly impaired the learning during conditioning trials, as well as the memory formation of bees at 2, 12, and 24 h after topical and oral exposure. Thus, deltamethrin inhibits learning, and bees were unable to memorize the learned task.
[Abuagla, M. I. B., Iqbal, J., Raweh, H. S. A., & Alqarni, A. S. (2024). Olfactory Learning Behavior and Mortality of the Honey Bee Apis mellifera jemenitica in Response to Pyrethroid Insecticide (Deltamethrin). Toxics, 12(1), 25. https://doi.org/10.3390/toxics12010025]
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. ]
The agricultural intensification represents a major threat to biodiversity, with negative effects on the ecosystem. In particular, habitat loss and degradation, along with pesticide use have been recognised as primary factors contributing to the actual global decline of pollinators. Here we investigated the quality of agroecosystems in the Emilia-Romagna region (Northern Italy) within the national monitoring project BeeNet. We analysed pesticide residues in 100 samples of beebread collected in 25 BeeNet stations in March and June 2021 and 2022. We evaluated diversity and concentration of these chemicals, their risk (TWC) to honey bees, and their correlation with land use. Overall, in 84 % of the samples we found 63 out of 373 different pesticide residues, >90 % of them belonging to fungicides and insecticides. The TWC exceeded the risk threshold in seven samples (TWCmix), mostly due to only one or two compounds. We also found 15 compounds not approved in the EU as plant protection products (PPPs), raising concerns about illegal use or contamination through beeswax recycling. Samples collected in 2021 and in June presented a significantly higher number of active ingredients and TWC than those collected in 2022 and in March. The TWC calculated on single compounds (TWCcom) exceeded the risk threshold in case of four insecticides, namely carbaryl, fipronil, imidacloprid and thiamethoxam (although each detected in only one sample). Finally, both TWC and number of active ingredients were moderately or highly positively correlated with the percentage of area covered by orchards. Considering that we found on average more than five different molecules per sample, and that we ignored potential synergistic effects, the results of this work highlight the alarming situation regarding pesticide treatments and toxicity risk for bees linked to the current agricultural practices, and the need for implementing sustainable and pollinator-friendly strategies.
[Bogo, G. et al. (2024) Residues of agrochemicals in beebread as an indicator of landscape management, Science of The Total Environment. Available at: https://www.sciencedirect.com/science/article/abs/pii/S0048969724042232?via%3Dihub. ]
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. ]
Mounting evidence supporting the negative impacts of exposure to neonicotinoids on bees has prompted the registration of novel ‘bee-friendly’ insecticides for agricultural use. Flupyradifurone (FPF) is a butenolide insecticide that shares the same mode of action as neonicotinoids and has been assessed to be ‘practically non-toxic to adult honeybees' using current risk assessment procedures. However, these assessments overlook some routes of exposure specific to wild bees, such as contact with residues in soil for ground-nesters. Co-exposure with other pesticides may also lead to detrimental synergistic effects. In a fully crossed experiment, we assessed the possible lethal and sublethal effects of chronic exposure to two pesticides used on Cucurbita crops, the insecticide Sivanto Prime (FPF) and the fungicide Quadris Top (azoxystrobin and difenoconazole), alone or combined, on solitary ground-nesting squash bees (Xenoglossa pruinosa). Squash bees exposed to Quadris Top collected less pollen per flower visit, while Sivanto-exposed bees produced larger offspring. Pesticide co-exposure induced hyperactivity in female squash bees relative to both the control and single pesticide exposure, and reduced the number of emerging offspring per nest compared to individual pesticide treatments. This study demonstrates that ‘low-toxicity’ pesticides can adversely affect squash bees under field-realistic exposure, alone or in combination.
[Rondeau, S. and Raine, N. (2024) Single and combined exposure to ‘bee safe’ pesticides alter behaviour and offspring production in a ground-nesting solitary bee (Xenoglossa pruinosa), Proceedings of the Royal Society Biological Sciences. Available at: https://royalsocietypublishing.org/doi/10.1098/rspb.2023.2939. ]
Bumblebees and other key pollinators are experiencing global declines, a phenomenon driven by multiple environmental stressors, including pesticide exposure. While bumblebee queens spend most of their life hibernating underground, no study to date has examined how exposure to pesticide-contaminated soils might affect bumblebee queens during this solitary phase of their lifecycle. We exposed Bombus impatiens queens (n = 303) to soil treated with field-realistic concentrations of two diamide insecticides (chlorantraniliprole and cyantraniliprole) and two fungicides (boscalid and difenoconazole), alone or combined, during a 30-week hibernation period. We found that exposure to boscalid residues in soil doubled the likelihood of queens surviving through the colony initiation period (after successful hibernation) and laying eggs. Our data also revealed complex interactions between pesticide exposure and queen body mass on aspects of colony founding. Among others, exposure to cyantraniliprole led to lethal and sublethal post-hibernation effects that were dependent on queen size, with larger queens showing higher mortality rates, delayed emergence of their first brood, and producing smaller workers. Our results show that effects of pesticide exposure depend on intrinsic traits of bumblebee queen physiology and challenge our understanding of how bees respond to pesticides under environmentally realistic exposure scenarios.
[Rondeau, S. and Raine, N. (2024) Size-dependent responses of colony-founding bumblebee (Bombus impatiens) queens to exposure to pesticide residues in soil during hibernation, The Science of the Total Environment. Available at: https://pubmed.ncbi.nlm.nih.gov/39029756/. ]
Biodiversity loss is accelerating, yet we know little about how these ecosystem disruptions affect human well-being. Ecologists have documented both the importance of bats as natural predators of insects as well as their population declines after the emergence of a wildlife disease, resulting in a potential decline in biological pest control. In this work, I study how species interactions can extend beyond an ecosystem and affect agriculture and human health. I find that farmers compensated for bat decline by increasing their insecticide use by 31.1%. The compensatory increase in insecticide use by farmers adversely affected health—human infant mortality increased by 7.9% in the counties that experienced bat die-offs. These findings provide empirical validation to previous theoretical predictions about how ecosystem disruptions can have meaningful social costs.
[Frank, E. (2024) The economic impacts of ecosystem disruptions: Costs from substituting biological pest control, Science. Available at: https://www.science.org/doi/10.1126/science.adg0344.]
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.]
Bee pollen is a food supplement that is receiving increasing attention for its nutraceutical and therapeutic properties. However, several uncertainties on the safety of this beekeeping product still exist. The present work addressed this issue through the critical evaluation of 61 studies, published over the 2014–2024 period, and focused on the analysis of pesticides and mycotoxins in bee pollen. A comprehensive examination of the analytical procedures employed for the analysis of these contaminants was performed. Overall, 358 pesticides and 7 mycotoxins were found in bee pollen, with certain compounds being globally distributed and frequently encountered. An overview of the existing European regulations concerning pesticide and mycotoxin levels in food was presented, emphasizing the exclusion of bee pollen from the list of monitored commodities. The findings of the reviewed studies revealed the necessity of gathering more data on bee pollen's contamination and consumption, in order to finally perform reliable risk assessments.
[Carrera, M. et al. (2024) Unveiling bee pollen’s contamination with pesticides and mycotoxins: Current analytical procedures, results and regulation, Trends in Analytical Chemistry. Available at: https://www.sciencedirect.com/science/article/abs/pii/S0165993624004187.]
With the long-term goal of exploring the viability of conservation biological control of cabbage aphid Brevicoryne brassicae (L.) (Hemiptera: Aphididae) in the northeastern United States, adult syrphid flies (Diptera: Syrphidae) were observed on several species of annual insectary plants at farm sites in Connecticut, Massachusetts, and New Hampshire. Insectary plant species included alyssum, Lobularia maritima (L.) (Brassicales: Brassicaceae), buckwheat, Fagopyrum esculentum (Moench) (Caryophyllales: Polygonaceae), phacelia, Phacelia tanacetifolia (Bentham) (Boraginales: Hydrophyllaceae), calendula, Calendula officinalis (L.) (Asterales: Asteraceae) and ammi, Ammi majus (L.) (Apiales: Apiaceae). Among these insectary plants, alyssum had the longest bloom period and attracted the most syrphids. We identified 21 species of syrphid flies from insectary plants. The three most prevalent species collected were the aphidophagous Toxomerus marginatus (Say) (Diptera: Syrphidae) (70.1% of samples) and T. geminatus (Say) (Diptera: Syrphidae) (8.8% of samples), as well as the non-aphidophagous Syritta pipiens (L.) (Diptera: Syrphidae) (13.1% of samples). The benefits of including these insectary plant species as a companion to Brassica (L.) (Brassicales: Brassicaceae) cropping systems are discussed.
[Harris-Cypher, A., Roman, C., Higgins, G., Scheufele, S., Legrand, A., Wallingford, A. and Sideman, R.G., 2023. Environmental Entomology, 52(2), pp.175-182.]
Excessive use of azole fungicides in agriculture poses a potential threat to honeybees and other pollinator insects; however, the detailed effects of these molecules remain largely unclear. Hence, in the present study it was aimed to investigate the acute sublethal effects of tebuconazole on the redox homeostasis and fatty acid composition in the brain of honeybees. Our findings demonstrate that tebuconazole decreased total antioxidant capacity, the ratio of reduced to oxidized glutathione and disturbed the function of key antioxidant defense enzymes along with the induction of lipid peroxidation indicated by increased malondialdehyde levels, while it also altered the fatty acid profile of the brain. The present study highlights the negative impact of tebuconazole on honeybees and contributes to the understanding of potential consequences related to azole exposure on pollinator insects' health, such as the occurrence of colony collapse disorder.
[Mackei, M., Sebők, C., Vöröházi, J., Tráj, P., Mackei, F., Oláh, B., Fébel, H., Neogrády, Z. and Mátis, G., 2023. Insect Biochemistry and Molecular Biology, 159, p.103990.]
Exposure to insecticides may contribute to global insect declines due to sublethal insecticide effects on non-target species. Thus far, much research on non-target insecticide effects has focused on neonicotinoids in a few bee species. Much less is known about effects on other insect taxa or newer insecticides, such as sulfoxaflor. Here, we studied the effects of an acute insecticide exposure on both olfactory and visual learning in free-moving Polistes fuscatus paper wasps. Wasps were exposed to a single, field-realistic oral dose of low-dose imidacloprid, high-dose imidacloprid or sulfoxaflor. Then, visual and olfactory learning and short-term memory were assessed. We found that acute insecticide exposure influenced performance, as sulfoxaflor- and high-dose imidacloprid-exposed wasps made fewer correct choices than control wasps. Notably, both visual and olfactory performance were similarly impaired. Wasps treated with high-dose imidacloprid were also less likely to complete the learning assay than wasps from the other treatment groups. Instead, wasps remained stationary and unmoving in the testing area, consistent with imidacloprid interfering with motor control. Finally, wasps treated with sulfoxaflor were more likely to die in the week after treatment than wasps in the other treatment groups. Our findings demonstrate that sublethal, field-realistic dosages of both neonicotinoid- and sulfoximine-based insecticides impair wasp learning and short-term memory, which may have additional effects on survival and motor functioning. Insecticides have broadly detrimental effects on diverse non-target insects that may influence foraging effectiveness, pollination services and ecosystem function.
[Fiona E. Corcoran, Elizabeth A. Tibbetts; Field-realistic exposure to neonicotinoid and sulfoximine insecticides impairs visual and olfactory learning and memory in Polistes paper wasps. J Exp Biol 15 November 2023; 226 (22): jeb246083. doi: https://doi.org/10.1242/jeb.246083]
Agrochemicals represent prominent anthropogenic stressors contributing to the ongoing global insect decline. While their impact is generally assessed in terms of mortality rates, non-lethal effects on fitness are equally important to insect conservation. Glyphosate, a commonly used herbicide, is toxic to many animal species, and thought to impact a range of physiological functions. In this study, we investigate the impact of long-term exposure to glyphosate on locomotion, phototaxis and learning abilities in bumblebees, using a fully automated high-throughput assay. We find that glyphosate exposure had a very slight and transient impact on locomotion, while leaving the phototactic drive unaffected. Glyphosate exposure also reduced attraction towards UV light when blue was given as an alternative and, most strikingly, impaired learning of aversive stimuli. Thus, glyphosate had specific actions on sensory and cognitive processes. These non-lethal perceptual and cognitive impairments likely represent a significant obstacle to foraging and predator avoidance for wild bumblebees exposed to glyphosate. Similar effects in other species could contribute to a widespread reduction in foraging efficiency across ecosystems, driven by the large-scale application of this herbicide. The high-throughput paradigm presented in this study can be adapted to investigate sublethal effects of other agrochemicals on bumblebees or other important pollinator species, opening up a critical new avenue for the study of anthropogenic stressors.
[Nouvian, M., Foster, J.J. and Weidenmüller, A., 2023. Science of the Total Environment, 898, p.165527.]
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.]
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. ]
Due to pollinator decline observed worldwide, many studies have been conducted on the pesticide residue content of apicultural products including bee bread, propolis, beeswax and royal jelly. These products are consumed for their nutraceutical properties, although, little information is available on the human health risk posed by pesticides present in them. In our research, studies dealing with the pesticide contamination of the above-mentioned hive products are reviewed. Dietary exposures were calculated based on the recommended daily intake values and concentration data reported by scientific studies. Potential acute and chronic health risk of consumers were evaluated by comparing the exposure values with health-based guidance values. Available data indicate that a wide range of pesticide residues, especially acaricides may accumulate in bee bread, propolis and beeswax, up to concentration levels of more thousand μg/kg. Based on our observations, tau-fluvalinate, coumaphos, chlorfenvinphos, chlorpyrifos and amitraz are commonly detected pesticide active substances in beehive products. Our estimates suggest that coumaphos and chlorfenvinphos can accumulate in beeswax to an extent that pose a potential health risk to the consumers of comb honey. However, it appears that pesticide residues do not transfer to royal jelly, presumably due to the filtering activity of nurse bees during secretion.
[Végh, R., Csóka, M., Mednyánszky, Z. and Sipos, L., 2023. Food and Chemical Toxicology, p.113806.]Abstract
[Nicholson, C.C. et al. (2023) ‘Pesticide use negatively affects bumble bees across European landscapes’, Nature [Preprint]. doi:10.1038/s41586-023-06773-3. ]
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.]
Climate change and agricultural intensification are exposing insect pollinators to temperature extremes and increasing pesticide usage. Yet, we lack good quantification of how temperature modulates the sublethal effects of pesticides on behaviours vital for fitness and pollination performance. Consequently, we are uncertain if warming decreases or increases the severity of different pesticide impacts, and whether separate behaviours vary in the direction of response. Quantifying these interactive effects is vital in forecasting pesticide risk across climate regions and informing pesticide application strategies and pollinator conservation. This multi-stressor study investigated the responses of six functional behaviours of bumblebees when exposed to either a neonicotinoid (imidacloprid) or a sulfoximine (sulfoxaflor) across a standardised low, mid, and high temperature. We found the neonicotinoid had a significant effect on five of the six behaviours, with a greater effect at the lower temperature(s) when measuring responsiveness, the likelihood of movement, walking rate, and food consumption rate. In contrast, the neonicotinoid had a greater impact on flight distance at the higher temperature. Our findings show that different organismal functions can exhibit divergent thermal responses, with some pesticide-affected behaviours showing greater impact as temperatures dropped, and others as temperatures rose. We must therefore account for environmental context when determining pesticide risk. Moreover, we found evidence of synergistic effects, with just a 3°C increase causing a sudden drop in flight performance, despite seeing no effect of pesticide at the two lower temperatures. Our findings highlight the importance of multi-stressor studies to quantify threats to insects, which will help to improve dynamic evaluations of population tipping points and spatiotemporal risks to biodiversity across different climate regions.
[Kenna, D., Graystock, P. and Gill, R.J., 2023..Global Change Biology.]
Bumble bees (genus Bombus) are important pollinators with more than 260 spe -cies found worldwide, many of which are in decline. Twenty-five species occur in California with the highest species abundance and diversity found in coastal, north -ern, and montane regions. No recent studies have examined California bumble bee di -versity across large spatial scales nor explored contemporary community composition patterns across the state. To fill these gaps, we collected 1740 bumble bee individuals, representing 17 species from 17 sites (~100 bees per site) in California, using an as -semblage monitoring framework. This framework is intended to provide an accurate estimate of relative abundance of more common species without negatively impact -ing populations through overcollection. Our sites were distributed across six ecore -gions, with an emphasis on those that historically hosted high bumble bee diversity. We compared bumble bee composition among these sites to provide a snapshot of California bumble bee biodiversity in a single year. Overall, the assemblage monitor-ing framework that we employed successfully captured estimated relative abundance of species for most sites, but not all. This shortcoming suggests that bumble bee biodiversity monitoring in California might require multiple monitoring approaches, including greater depth of sampling in some regions, given the variable patterns in bumble bee abundance and richness throughout the state. Our study sheds light on the current status of bumble bee diversity in California, identifies some areas where greater sampling effort and conservation action should be focused in the future, and performs the first assessment of an assembly monitoring framework for bumble bee communities in the state.
[Fisher, K., Watrous, K.M., Williams, N.M., Richardson, L.L. and Woodard, S.H. Ecology and Evolution, 12(3), p.e8505.]
Honeybee health and the species’ gut microbiota are interconnected. Also noteworthy are the multiple niches present within hives, each with distinct microbiotas and all coexisting, which we termed “apibiome”. External stressors (e.g. anthropization) can compromise microbial balance and bee resilience. We hypothesised that (1) the bacterial communities of hives located in areas with different degrees of anthropization differ in composition, and (2) due to interactions between the multiple microbiomes within the apibiome, changes in the community of a niche would impact the bacteria present in other hive sections. We characterised the bacterial consortia of different niches (bee gut, bee bread, hive entrance and internal hive air) of 43 hives from 3 different environments (agricultural, semi-natural and natural) through 16S rRNA amplicon sequencing. Agricultural samples presented lower community evenness, depletion of beneficial bacteria, and increased recruitment of stress related pathways (predicted via PICRUSt2). The taxonomic and functional composition of gut and hive entrance followed an environmental gradient. Arsenophonus emerged as a possible indicator of anthropization, gradually decreasing in abundance from agriculture to the natural environment in multiple niches. Importantly, after 16 days of exposure to a semi-natural landscape hives showed intermediate profiles, suggesting alleviation of microbial dysbiosis through reduction of anthropization.
[Gorrochategui-Ortega, J., Muñoz-Colmenero, M., Kovačić, M., Filipi, J., Puškadija, Z., Kezić, N., Parejo, M., Büchler, R., Estonba, A. and Zarraonaindia, I., 2022.Scientific Reports, 12(1), p.18832.]
Flumethrin is one of the few acaricides that permit the control of Varroa disease or varroosis in bee colonies. However, flumethrin accumulates in hive products. We previously discovered that sublethal doses of flumethrin induce significant physiological stress in honeybees (Apis mellifera L.), however its potential impacts on the honeybee gut microenvironment remains unknown. To fill this gap, honeybees were exposed to a field-relevant concentration of flumethrin (10 μg/L) for 14 d and its potential impacts on gut system were evaluated. The results indicated that flumethrin triggered immune responses in the gut but had limited effects on survival and gut microbial composition. However, survival stress drastically increased in bees exposed to antibiotics, suggesting that the gut microbiota is closely related to flumethrin-induced dysbiosis in the bee gut. Based on a non-targeted metabolomics approach, flumethrin at 10 μg/L considerably altered the composition of intestinal metabolites, and we discovered that this metabolic stress was closely linked with a reduction of gut core bacterial endosymbiont Gilliamella spp. through a combination of microbiological and metabolomics investigations. Finally, an in vitro study showed that while flumethrin does not directly inhibit the growth of Gilliamella apicola isolates, it does have a significant impact on the glycerophospholipid metabolism in bacteria cells, which was also observed in host bees. These findings indicated that even though flumethrin administered at environmental relevant concentrations does not significantly induce death in honeybees, it still alters the metabolism balance between honeybees and the gut symbiotic bacterium, G. apicola. The considerable negative impact of flumethrin on the honeybee gut microenvironment emphasizes the importance of properly monitoring acaricide to avoid potential environmental concerns, and further studies are needed to illustrate the mode of action of bee health-gut microbiota-exogenous pesticides.
[Qi, S., Al Naggar, Y., Li, J., Liu, Z., Xue, X., Wu, L., El-Seedi, H.R. and Wang, K., 2022. Chemosphere, 307, p.136030.]
The gut microbiome plays an important role in bee health and disease. But it can be disrupted by pesticides and in-hive chemicals, putting honey bee health in danger. We used a controlled and fully crossed laboratory experimental design to test the effects of a 10-day period of chronic exposure to field-realistic sublethal concentrations of two nicotinic acetylcholine receptor agonist insecticides (nACHRs), namely flupyradifurone (FPF) and sulfoxaflor (Sulf), and a fungicide, azoxystrobin (Azoxy), individually and in combination, on the survival of individual honey bee workers and the composition of their gut microbiota (fungal and bacterial diversity). Metabarcoding was used to examine the gut microbiota on days 0, 5, and 10 of pesticide exposure to determine how the microbial response varies over time; to do so, the fungal ITS2 fragment and the V4 region of the bacterial 16S rRNA were targeted. We found that FPF has a negative impact on honey bee survival, but interactive (additive or synergistic) effects between either insecticide and the fungicide on honey bee survival were not statistically significant. Pesticide treatments significantly impacted the microbial community composition. The fungicide Azoxy substantially reduced the Shannon diversity of fungi after chronic exposure for 10 days. The relative abundance of the top 10 genera of the bee gut microbiota was also differentially affected by the fungicide, insecticides, and fungicide-insecticide combinations. Gut microbiota dysbiosis was associated with an increase in the relative abundance of opportunistic pathogens such as Serratia spp. (e.g. S. marcescens), which can have devastating consequences for host health such as increased susceptibility to infection and reduced lifespan. Our findings raise concerns about the long-term impact of novel nACHR insecticides, particularly FPF, on pollinator health and recommend a novel methodology for a refined risk assessment that includes the potential effects of agrochemicals on the gut microbiome of bees.
The gut microbiome plays an important role in bee health and disease. But it can be disrupted by pesticides and in-hive chemicals, putting honey bee health in danger. We used a controlled and fully crossed laboratory experimental design to test the effects of a 10-day period of chronic exposure to field-realistic sublethal concentrations of two nicotinic acetylcholine receptor agonist insecticides (nACHRs), namely flupyradifurone (FPF) and sulfoxaflor (Sulf), and a fungicide, azoxystrobin (Azoxy), individually and in combination, on the survival of individual honey bee workers and the composition of their gut microbiota (fungal and bacterial diversity). Metabarcoding was used to examine the gut microbiota on days 0, 5, and 10 of pesticide exposure to determine how the microbial response varies over time; to do so, the fungal ITS2 fragment and the V4 region of the bacterial 16S rRNA were targeted. We found that FPF has a negative impact on honey bee survival, but interactive (additive or synergistic) effects between either insecticide and the fungicide on honey bee survival were not statistically significant. Pesticide treatments significantly impacted the microbial community composition. The fungicide Azoxy substantially reduced the Shannon diversity of fungi after chronic exposure for 10 days. The relative abundance of the top 10 genera of the bee gut microbiota was also differentially affected by the fungicide, insecticides, and fungicide-insecticide combinations. Gut microbiota dysbiosis was associated with an increase in the relative abundance of opportunistic pathogens such as Serratia spp. (e.g. S. marcescens), which can have devastating consequences for host health such as increased susceptibility to infection and reduced lifespan. Our findings raise concerns about the long-term impact of novel nACHR insecticides, particularly FPF, on pollinator health and recommend a novel methodology for a refined risk assessment that includes the potential effects of agrochemicals on the gut microbiome of bees.
[Al Naggar, Y., Singavarapu, B., Paxton, R.J. and Wubet, T., 2022. Science of The Total Environment, 849, p.157941.]
Fungicides account for more than 35% of the global pesticide market and their use is predicted to increase in the future. While fungicides are commonly applied during bloom when bees are likely foraging on crops, whether real-world exposure to these chemicals - alone or in combination with other stressors - constitutes a threat to the health of bees is still the subject of great uncertainty. The first step in estimating the risks of exposure to fungicides for bees is to understand how and to what extent bees are exposed to these active ingredients. Here we review the current knowledge that exists about exposure to fungicides that bees experience in the field, and link quantitative data on exposure to acute and chronic risk of lethal endpoints for honey bees (Apis mellifera). From the 702 publications we screened, 76 studies contained quantitative data on residue detections in honey bee matrices, and a further 47 provided qualitative information about exposure for a range of bee taxa through various routes. We compiled data for 90 fungicides and metabolites that have been detected in honey, beebread, pollen, beeswax, and the bodies of honey bees. The risks posed to honey bees by fungicide residues was estimated through the EPA Risk Quotient (RQ) approach. Based on residue concentrations detected in honey and pollen/beebread, none of the reported fungicides exceeded the levels of concern (LOC) set by regulatory agencies for acute risk, while 3 and 12 fungicides exceeded the European Food Safety Authority (EFSA) chronic LOC for honey bees and wild bees, respectively. When considering exposure to all bees, fungicides of most concern include many broad-spectrum systemic fungicides, as well as the widely used broad-spectrum contact fungicide chlorothalonil. In addition to providing a detailed overview of the frequency and extent of fungicide residue detections in the bee environment, we identified important research gaps and suggest future directions to move towards a more comprehensive understanding and mitigation of the risks of exposure to fungicides for bees, including synergistic risks of co-exposure to fungicides and other pesticides or pathogens.
[Rondeau, S. and Raine, N. (2022) Fungicides and bees: a review of exposure and risk, Environment international. Available at: https://pubmed.ncbi.nlm.nih.gov/35714526/. ]
Insects are facing a multitude of anthropogenic stressors, and the recent decline in their biodiversity is threatening ecosystems and economies across the globe. We investigated the impact of glyphosate, the most commonly used herbicide worldwide, on bumblebees. Bumblebee colonies maintain their brood at high temperatures via active thermogenesis, a prerequisite for colony growth and reproduction. Using a within-colony comparative approach to examine the effects of long-term glyphosate exposure on both individual and collective thermoregulation, we found that whereas effects are weak at the level of the individual, the collective ability to maintain the necessary high brood temperatures is decreased by more than 25% during periods of resource limitation. For pollinators in our heavily stressed ecosystems, glyphosate exposure carries hidden costs that have so far been largely overlooked.
[Weidenmüller, A., Meltzer, A., Neupert, S., Schwarz, A. and Kleineidam, C. Science, 376(6597), pp.1122-1126.]
A field spray drift experiment using florpyrauxifen-benzyl was conducted to measure drift from commercial ground and aerial applications, evaluate soybean [Glycine max (L.) Merr.] impacts, and compare to United States Environmental Protection Agency (US EPA) drift models. Collected field data were consistent with US EPA model predictions. Generally, with both systems applying a Coarse spray in a 13-kph average wind speed, the aerial application had a 5.0- to 8.6-fold increase in drift compared to the ground application, and subsequently, a 1.7- to 3.6-fold increase in downwind soybean injury. Soybean reproductive structures were severely reduced following herbicide exposure, potentially negatively impacting pollinator foraging sources. Approximately a 25% reduction of reproductive structures up to 30.5-m downwind and nearly a 100% reduction at 61-m downwind were observed for ground and aerial applications, respectively. Aerial applications would require three to five swath width adjustments upwind to reduce drift potential similar to ground applications.
[Butts, T.R., Fritz, B.K., Kouame, K., Norsworthy, J.K., Barber, L.T., Ross, W.J., Lorenz, G.M., Thrash, B.C., Bateman, N.R. and Adamczyk, J.J., 2022. Scientific Reports, 12(1), pp.1-15.]
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. ]
Social bee gut microbiotas play key roles in host health and performance. Worryingly, a growing body of literature shows that pesticide exposure can disturb these microbiotas. Most studies examine changes in taxonomic composition in Western honey bee (Apis mellifera) gut microbiotas caused by insecticide exposure. Core bee gut microbiota taxa shift in abundance after exposure but are rarely eliminated, with declines in Bifidobacteriales and Lactobacillus near melliventris abundance being the most common shifts. Pesticide concentration, exposure duration, season and concurrent stressors all influence whether and how bee gut microbiotas are disturbed. Also, the mechanism of disturbance—i.e. whether a pesticide directly affects microbial growth or indirectly affects the microbiota by altering host health—likely affects disturbance consistency. Despite growing interest in this topic, important questions remain unanswered. Specifically, metabolic shifts in bee gut microbiotas remain largely uninvestigated, as do effects of pesticide-disturbed gut microbiotas on bee host performance. Furthermore, few bee species have been studied other than A. mellifera, and few herbicides and fungicides have been examined. We call for these knowledge gaps to be addressed so that we may obtain a comprehensive picture of how pesticides alter bee gut microbiotas, and of the functional consequences of these changes.
[Hotchkiss, M.Z., Poulain, A.J. and Forrest, J.R. FEMS Microbiology Reviews, 46(2), p.fuab056.]
Wild and managed pollinators are essential to food production and the function of natural ecosystems; however, their populations are threatened by multiple stressors including pesticide use. Because pollinator species can travel hundreds to thousands of meters to forage, recent research has stressed the importance of evaluating pollinator decline at the landscape scale. However, scientists’ and conservationists’ ability to do this has been limited by a lack of accessible data on pesticide use at relevant spatial scales and in toxicological units meaningful to pollinators. Here, we synthesize information from several large, publicly available datasets on pesticide use patterns, land use, and toxicity to generate novel datasets describing pesticide use by active ingredient (kg, 1997–2017) and aggregate insecticide load (kg and honey bee lethal doses, 1997–2014) for state-crop combinations in the contiguous U.S. Furthermore, by linking pesticide datasets with land-use data, we describe a method to map pesticide indicators at spatial scales relevant to pollinator research and conservation.
[Douglas, M.R., Baisley, P., Soba, S., Kammerer, M., Lonsdorf, E.V. and Grozinger, C.M., 2022. Scientific Data, 9(1), pp.1-15.]
Exposure to pesticides is a major threat to bumblebee (Bombus spp.) health. In temperate regions, queens of many bumblebee species hibernate underground for several months, putting them at potentially high risk of exposure to soil contaminants. The extent to which bumblebees are exposed to residues in agricultural soils during hibernation is currently unknown, which limits our understanding of the full pesticide exposome for bumblebees throughout their lifecycle. To generate field exposure estimates for overwintering bumblebee queens to pesticide residues, we sampled soils from areas corresponding to suitable likely hibernation sites at six apple orchards and 13 diversified farms throughout Southern Ontario (Canada) in fall 2019-2020. Detectable levels of pesticides were found in 65 of 66 soil samples analysed for multi-pesticide residues (UPLC-MS/MS). A total of 53 active ingredients (AIs) were detected in soils, including 27 fungicides, 13 insecticides, and 13 herbicides. Overall, the frequency of detection, residue levels (median = 37.82 vs. 2.20 ng/g), and number of pesticides per sample (mean = 12 vs. 4 AIs) were highest for orchard soils compared to soils from diversified farms. Ninety-one percent of samples contained multiple residues (up to 29 different AIs per sample), including mixtures of insecticides and fungicides that might lead to synergistic effects. Our results suggest that when hibernating in agricultural areas, bumblebee queens are very likely to be exposed to a wide range of pesticide residues in soil, including potentially harmful levels of insecticides (e.g., cyantraniliprole up to 148.82 ng/g). Our study indicates the importance of empirically testing the potential effects of pesticide residues in soils for hibernating bumblebee queens, using field exposure data such as those generated here. The differences in potential exposure that we detected between cropping systems can also be used to better inform regulations that govern the use of agricultural pesticides, notably in apple orchards.
[Rondeau, S. et al. (2022) Quantifying exposure of bumblebee (Bombus spp.) queens to pesticide residues when hibernating in agricultural soils, Environmental Pollution. Available at: https://pubmed.ncbi.nlm.nih.gov/35809712/. ]
Flumethrin is a highly effective acaricide, but its lipophilic characteristic has some negative effects, such as accumulation in bee hives and bee products. However, studies on the survival stress of honey bees subsequent to chronic flumethrin exposure are limited. To answer this question, a study was carried out on the stress to honey bee (Apis mellifera) workers from larvae to adults by chronic exposure to sublethal concentrations of flumethrin. Three flumethrin treatment groups (1, 0.1, 0.01 mg/L) and one control group (with no added flumethrin) were established and divided the worker larvae into four groups. Then, starting with 2-day-old larvae, larvae and subsequent emerged worker bees of the four groups were orally fed with the corresponding concentrations of flumethrin until all the adult worker bees died, respectively. When the concentration was at 0.01 mg/L of flumethrin, the lifespan of adult worker bees decreased, and a down-regulation of detoxification-related genes (CYP450,GSTS) was induced in 1-day-old pupae. When it is at 0.1 mg/L flumethrin, the lifespan of adult worker bees was again shortened, and down-regulation of memory-related genes (GluRA1, Nmdar1, Tyr1) in 1-day-old pupae and gene Tyr1 in 1-day-old worker bees, detoxification-related genes (CYP450,GSTS) in 1-day-old pupae, and immunity genes (Defensin1, Hymenoptaecin) in 7-day-old worker bees were observed. When the concentration is at 1 mg/L flumethrin, lighter birth weight of newly emerged honeybee was found and deficiencies in olfactory learning and memory were observed in 7-day-old worker bees. Memory-related genes (GluRA1, Nmdar1, Tyr1) were down-regulated in 1-day-old pupae and genes (Nmdar1,Tyr1)in 1-day-old worker bees, as were detoxification-related genes (CYP450,GSTS) in 1-day-old pupae and gene CPY450 in 7-day-old worker bees, and immune genes (Defensin1, Hymenoptaecin) in 7-day-old worker bees. There was no significant difference in pupal weight, capping rate, emergence rate, expression of immune-related genes of 1-day-old pupae, expression of immune-related genes and detoxification-related genes of 1-day-old worker bees, expression of memory-related genes and detoxification-related gene GSTS of 7-day-old worker bees. These data provide an ominous warning about the unintended consequences on apiaries, and underscore the need for careful control of flumethrin residues in bee hives.
[Zhen Li, Heyan Yang, Longtao Yu, Chen Liu, Xiaobo Wu, The negative effect of flumethrin stress on honey bee (Apis mellifera) worker from larvae to adults, Pesticide Biochemistry and Physiology, Volume 188, 2022, 105289, ISSN 0048-3575, https://doi.org/10.1016/j.pestbp.2022.105289.]
Residential gardens are a valuable habitat for insect pollinators worldwide, but differences in individual gardening practices substantially affect their floral composition. It is important to understand how the floral resource supply of gardens varies in both space and time so we can develop evidence-based management recommendations to support pollinator conservation in towns and cities.
We surveyed 59 residential gardens in the city of Bristol, UK, at monthly intervals from March to October. For each of 472 garden surveys, we combined floral abundances with nectar sugar data to quantify the nectar production of each garden, investigating the magnitude, temporal stability, and diversity and composition of garden nectar supplies.
We found that individual gardens differ markedly in the quantity of nectar sugar they supply (from 2 to 1,662 g), and nectar production is higher in more affluent neighbourhoods, but not in larger gardens. Nectar supply peaks in July (mid-summer), when more plant taxa are in flower, but temporal patterns vary among individual gardens. At larger spatial scales, temporal variability averages out through the portfolio effect, meaning insect pollinators foraging across many gardens in urban landscapes have access to a relatively stable and continuous supply of nectar through the year.
Turnover in species composition among gardens leads to an extremely high overall plant richness, with 636 taxa recorded flowering. The nectar supply is dominated by non-natives, which provide 91% of all nectar sugar, while shrubs are the main plant life form contributing to nectar production (58%). Two-thirds of nectar sugar is only available to relatively specialised pollinators, leaving just one-third that is accessible to all.
Synthesis and applications. By measuring nectar supply in residential gardens, our study demonstrates that pollinator-friendly management, affecting garden quality, is more important than the size of a garden, giving every gardener an opportunity to contribute to pollinator conservation in urban areas. For gardeners interested in increasing the value of their land to foraging pollinators, we recommend planting nectar-rich shrubs with complementary flowering periods and prioritising flowers with an open structure in late summer and autumn.
[Tew, N.E., Baldock, K.C., Vaughan, I.P., Bird, S. and Memmott, J. Journal of Applied Ecology, 59(3), pp.801-811.]
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. ]
Pollinators, particularly wild bees, are suffering declines across the globe, and pesticides are thought to be drivers of these declines. Research into, and regulation of pesticides has focused on the active ingredients, and their impact on bee health. In contrast, the additional components in pesticide formulations have been overlooked as potential threats. By testing an acute oral dose of the fungicide product Amistar, and equivalent doses of each individual co-formulant, we were able to measure the toxicity of the formulation and identify the ingredient responsible. We found that a co-formulant, alcohol ethoxylates, caused a range of damage to bumble bee health. Exposure to alcohol ethoxylates caused 30% mortality and a range of sublethal effects. Alcohol ethoxylates treated bees consumed half as much sucrose as negative control bees over the course of the experiment and lost weight. Alcohol ethoxylates treated bees had significant melanisation of their midguts, evidence of gut damage. We suggest that this gut damage explains the reduction in appetite, weight loss and mortality, with bees dying from energy depletion. Our results demonstrate that sublethal impacts of pesticide formulations need to be considered during regulatory consideration, and that co-formulants can be more toxic than active ingredients.
[Straw, E.A. and Brown, M.J. Scientific reports, 11(1), pp.1-10.]
Pesticides are linked to global insect declines, with impacts on biodiversity and essential ecosystem services. In addition to well-documented direct impacts of pesticides at the current stage or time, potential delayed “carryover” effects from past exposure at a different life stage may augment impacts on individuals and populations. We investigated the effects of current exposure and the carryover effects of past insecticide exposure on the individual vital rates and population growth of the solitary bee, Osmia lignaria. Bees in flight cages freely foraged on wildflowers, some treated with the common insecticide, imidacloprid, in a fully crossed design over 2 y, with insecticide exposure or no exposure in each year. Insecticide exposure directly to foraging adults and via carryover effects from past exposure reduced reproduction. Repeated exposure across 2 y additively impaired individual performance, leading to a nearly fourfold reduction in bee population growth. Exposure to even a single insecticide application can have persistent effects on vital rates and can reduce population growth for multiple generations. Carryover effects had profound implications for population persistence and must be considered in risk assessment, conservation, and management decisions for pollinators to mitigate the effects of insecticide exposure.
[Stuligross, C. and Williams, N.M. Proceedings of the National Academy of Sciences, 118(48).]
Establishment and maintenance of milkweed plants (Asclepias spp.) in agricultural landscapes of the north central United States are needed to reverse the decline of North America's eastern monarch butterfly (Danaus plexippus) population. Because of a lack of toxicity data, it is unclear how insecticide use may reduce monarch productivity when milkweed habitat is placed near maize and soybean fields. To assess the potential effects of foliar insecticides, acute cuticular and dietary toxicity of 5 representative active ingredients were determined: beta‐cyfluthrin (pyrethroid), chlorantraniliprole (anthranilic diamide), chlorpyrifos (organophosphate), and imidacloprid and thiamethoxam (neonicotinoids). Cuticular median lethal dose values for first instars ranged from 9.2 × 10–3 to 79 μg/g larvae for beta‐cyfluthrin and chlorpyrifos, respectively. Dietary median lethal concentration values for second instars ranged from 8.3 × 10–3 to 8.4 μg/g milkweed leaf for chlorantraniliprole and chlorpyrifos, respectively. To estimate larval mortality rates downwind from treated fields, modeled insecticide exposures to larvae and milkweed leaves were compared to dose–response curves obtained from bioassays with first‐, second‐, third‐, and fifth‐instar larvae. For aerial applications to manage soybean aphids, mortality rates at 60 m downwind were highest for beta‐cyfluthrin and chlorantraniliprole following cuticular and dietary exposure, respectively, and lowest for thiamethoxam. To estimate landscape‐scale risks, field‐scale mortality rates must be considered in the context of spatial and temporal patterns of insecticide use.
[Krishnan, N., Zhang, Y., Bidne, K.G., Hellmich, R.L., Coats, J.R. and Bradbury, S.P., 2020. Environmental Toxicology and Chemistry, 39(4), pp.923-941.]
Imidacloprid, a widely used neonicotinoid insecticide, has led to a decline in the honey bee population worldwide. An invertebrate insect prey with neonicotinoid toxicity can adversely affect insectivores, such as echolocating bats. The aim of the current study was to examined whether imidacloprid toxicity may interfere echolocation system such as vocal, auditory, orientation, and spatial memory systems in the insectivorous bat. By comparing the ultrasound spectrum, auditory brainstem-evoked potential, and flight trajectory, we found that imidacloprid toxicity may interfere functions in vocal, auditory, orientation, and spatial memory system of insectivorous bats (Hipposideros armiger terasensis). As suggested from immunohistochemistry and western blots evidences, we found that insectivorous bats after suffering imidacloprid toxicity may decrease vocal-related FOXP2 expressions in the superior colliculus, auditory-related prestin expressions in the cochlea, and the auditory-related otoferlin expressions in the cochlea and the inferior colliculus, and cause inflammation and mitochondrial dysfunction-related apoptosis in the hippocampal CA1 and medial entorhinal cortex. These results may provide a reasonable explanation about imidacloprid-induced interference of echolocation system in insectivorous bats.
[Chung-Hsin Wu, Ching-Lung Lin, Sheue-Er Wang, Chen-Wen Lu, Effects of imidacloprid, a neonicotinoid insecticide, on the echolocation system of insectivorous bats, Pesticide Biochemistry and Physiology, Volume 163, 2020, Pages 94-101, ISSN 0048-3575, https://doi.org/10.1016/j.pestbp.2019.10.010.]
Neonicotinoids are pesticides used to protect crops but with known secondary influences at sublethal doses on bees. Honeybees use their sense of smell to identify the queen and nestmates, to signal danger and to distinguish flowers during foraging. Few behavioural studies to date have examined how neonicotinoid pesticides affect the ability of bees to distinguish odours. Here, we used a differential learning task to test how neonicotinoid exposure affects learning, memory and olfactory perception in foraging-age honeybees. Bees fed with thiamethoxam could not perform differential learning and could not distinguish odours during short- and long-term memory tests. Our data indicate that thiamethoxam directly impacts the cognitive processes involved in working memory required during differential olfactory learning. Using a combination of behavioural assays, we also identified that thiamethoxam has a direct impact on the olfactory perception of similar odours. Honeybees fed with other neonicotinoids (clothianidin, imidacloprid, dinotefuran) performed the differential learning task, but at a slower rate than the control. These bees could also distinguish the odours. Our data are the first to show that neonicotinoids have compound specific effects on the ability of bees to perform a complex olfactory learning task. Deficits in decision making caused by thiamethoxam exposure could mean that this is more harmful than other neonicotinoids, leading to inefficient foraging and a reduced ability to identify nestmates.
[Julie A. Mustard, Annie Gott, Jennifer Scott, Nancy L. Chavarria, Geraldine A. Wright; Honeybees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide. J Exp Biol 1 March 2020; 223 (5): jeb217174. doi: https://doi.org/10.1242/jeb.217174]
Increased agricultural production has been increased use of pesticides worldwide, which poses a threat to both human and environmental health. Recent studies suggest that several non-target organisms, from bees to mammals, show a wide variety of toxic effects of pesticides exposure, including impaired behavior, development and reproduction. Among mammals, bats are usually a neglected taxon among ecotoxicological studies, although they play important ecological and economical roles in forest ecosystems and agriculture through to seed dispersal and insect population control. Considering their wide variety of food habits, bats are exposed to environmental pollutants through food or water contamination, or through direct skin contact in their roosting areas. In order to better understand the risk posed by pesticides to bats populations, we compiled studies that investigated the main toxicological effects of pesticides in bats, aiming at contributing to discussion about the environmental risks associated with the use of pesticides.
[Oliveira, J.M. et al. (2020) How do pesticides affect bats? – A brief review of recent publications, Brazilian Journal of Biology. Available at: https://www.scielo.br/j/bjb/a/tnNtGd6GfzQFz6yNXNdzJPw/?lang=en. ]
Bumblebees exposed to neonicotinoid pesticides collect less pollen on foraging trips. Exposed bumblebees are also slower to learn to handle flowers, which may account for reduced pollen collection. It is unclear, however, why neonicotinoid exposure slows learning to handle flowers. We investigated the effect of imidacloprid, a neonicotinoid pesticide, on bumblebee motor learning using a lab model of flower handling. Bumblebees learned to invert inside a narrow tube and lift a petal-shaped barrier to reach a reward chamber. Imidacloprid-exposed bumblebees showed a dose-dependent delay to solve the task, which resulted from reduced switching between behavioural strategies and a subsequent delay in use of the successful strategy. This effect was consistent in colonies exposed at 10 but not 2.6 ppb, suggesting a variable effect on individuals at lower doses. These results help to explain why exposed bumblebees are slow to learn to handle flowers and collect less pollen on foraging trips.
[Phelps, J.D., Strang, C.G. & Sherry, D.F. Imidacloprid impairs performance on a model flower handling task in bumblebees (Bombus impatiens). Ecotoxicology 29, 359–374 (2020). https://doi.org/10.1007/s10646-020-02182-8]
For social bees, an understudied step in evaluating pesticide risk is how contaminated food entering colonies affects residing offspring development and maturation. For instance, neurotoxic insecticide compounds in food could affect central nervous system development predisposing individuals to become poorer task performers later-in-life. Studying bumblebee colonies provisioned with neonicotinoid spiked nectar substitute, we measured brain volume and learning behaviour of 3 or 12-day old adults that had experienced in-hive exposure during brood and/or early-stage adult development. Micro-computed tomography scanning and segmentation of multiple brain neuropils showed exposure during either of the developmental stages caused reduced mushroom body calycal growth relative to unexposed workers. Associated with this was a lower probability of responding to a sucrose reward and lower learning performance in an olfactory conditioning test. While calycal volume of control workers positively correlated with learning score, this relationship was absent for exposed workers indicating neuropil functional impairment. Comparison of 3- and 12-day adults exposed during brood development showed a similar degree of reduced calycal volume and impaired behaviour highlighting lasting and irrecoverable effects from exposure despite no adult exposure. Our findings help explain how the onset of pesticide exposure to whole colonies can lead to lag-effects on growth and resultant dysfunction.
[Smith DB, Arce AN, Ramos Rodrigues A, Bischoff PH, Burris D, Ahmed F, Gill RJ. Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebees. Proc Biol Sci. 2020 Mar 11;287(1922):20192442. doi: 10.1098/rspb.2019.2442. Epub 2020 Mar 4. PMID: 32126960; PMCID: PMC7126076.]
Bats play a vital role in our ecosystems and economies as natural pest‐control agents, seed dispersers, and pollinators. Agricultural intensification, however, can impact bats foraging near crops, affecting the ecosystem services they provide. Exposure to pesticides, for example, may induce chromosome breakage or missegregation that can result in micronucleus formation. Detection of micronuclei is a simple, inexpensive, and relatively minimally invasive technique commonly used to evaluate chemical genotoxicity but rarely applied to assess wildlife genotoxic effects. We evaluated the suitability of the micronucleus test as a biomarker of genotoxicity for biomonitoring field studies in bats. We collected blood samples from insectivorous bats roosting in caves surrounded by different levels of disturbance (agriculture, human settlements) in Colima and Jalisco, west central Mexico. Then, we examined the frequency of micronucleus inclusions in erythrocytes using differentially stained blood smears. Bats from caves surrounded by proportionately more (53%) land used for agriculture and irrigated year‐round had higher micronucleus frequency than bats from a less disturbed site (15% agriculture). We conclude that the micronucleus test is a sensitive method to evaluate genotoxic effects in free‐ranging bats and could provide a useful biomarker for evaluating risk of exposure in wild populations. Environ Toxicol Chem 2021;40:202–207.
[Sandoval‐Herrera, N., Castillo, J.P., Montalvo, L.G.H. and Welch, K.C., 2020. Environmental Toxicology and Chemistry.]
Learning is important for honey bee fitness and the pollination services that they provide. Neonicotinoid pesticides impair learning, fitness, colony health, and pollination, but most studies on how they affect bee learning have focused on olfactory learning. We tested the effects of field realistic doses of 0.8 ng/bee and 1.34 ng/bee of the neonicotinoid pesticide, thiamethoxam (TMX), on bee visual learning. We adapted a T-maze bioassay and classically conditioned bees to associate sugar reward with a simulated flower color (blue or yellow light) in a choice assay. At 1.34 ng/bee, TMX significantly reduced correct choices in the final learning trial as compared to the control treatment. There was no TMX effect in our 1-h memory test. We found stronger effects on decision time and abnormal behaviors. TMX decreased bee decision times, a potential byproduct of induced hyperactivity since bees walked to make choices. Behaviors (falling, trembling, and rapid abnormal movements) were significantly increased by both TMX doses as compared to the control treatment. These results suggest that the effects of neonicotinoids on bee visual learning should be further studied and incorporated into Risk Assessment protocols.
[Joshua C. Ludicke, James C. Nieh, Thiamethoxam impairs honey bee visual learning, alters decision times, and increases abnormal behaviors, Ecotoxicology and Environmental Safety, Volume 193, 2020, 110367, ISSN 0147-6513, https://doi.org/10.1016/j.ecoenv.2020.110367.]
Declines in honey bee populations represent a worldwide concern. The widespread use of neonicotinoid insecticides has been one of the factors linked to these declines. Sublethal doses of a neonicotinoid insecticide, imidacloprid, has been reported to cause olfactory learning deficits in honey bees via impairment of the target organ, the brain. In the present study, olfactory learning of honey bees was compared between controls and imidacloprid-treated bees. The brains of imidacloprid-treated and control bees were used for comparative transcriptome analysis by RNA-Seq to elucidate the effects of imidacloprid on honey bee learning capacity. The results showed that the learning performance of imidacloprid-treated bees was significantly impaired in comparison with control bees after chronic oral exposure to imidacloprid (0.02 ng/μl) for 11 days. Gene expression profiles between imidacloprid treatment and the control revealed that 131 genes were differentially expressed, of which 130 were downregulated in imidacloprid-treated bees. Validation of the RNA-Seq data using qRT-PCR showed that the results of qRT-PCR and RNA-Seq exhibited a high level of agreement. Gene ontology annotation indicated that the oxidation-reduction imbalance might exist in the brain of honey bees due to oxidative stress induced by imidacloprid exposure. KEGG and ingenuity pathway analysis revealed that transient receptor potential and Arrestin 2 in the phototransduction pathway were significantly downregulated in imidacloprid-treated bees, and that five downregulated genes have causal effects on behavioral response inhibition in imidacloprid-treated bees. Our results suggest that downregulation of brain genes involved in immune, detoxification and chemosensory responses may result in decreased olfactory learning capabilities in imidacloprid-treated bees.
[Zhiguo Li, Tiantian Yu, Yanping Chen, Matthew Heerman, Jingfang He, Jingnan Huang, Hongyi Nie, Songkun Su, Brain transcriptome of honey bees (Apis mellifera) exhibiting impaired olfactory learning induced by a sublethal dose of imidacloprid, Pesticide Biochemistry and Physiology, Volume 156, 2019, Pages 36-43, ISSN 0048-3575, https://doi.org/10.1016/j.pestbp.2019.02.001.]
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. ]
Neonicotinoids act as agonists on the nicotinic Acetylcholine receptor (nAChR) in insect brains, an essential molecular component of central brain structures involved in learning and memory formation. Sublethal doses might, therefore, impair neural processes necessary for adaptive experience dependent behaviour and thus reduce the fitness of pollinating insects on the individual and community level. First, the question was addressed whether clothianidin has an aversive taste for honey bees and concluded with both a laboratory and a semi-field experiment that bees are unable to distinguish between control and contaminated sucrose solutions. In the laboratory, proboscis extension response conditioning was performed with forager bees exposed to different concentrations of clothianidin (0.1, 0.3 and 0.8 ng/bee) before learning, after learning during memory consolidation, and just before memory retention. These tests at different timings allowed uncovering an impairment of the consolidation and retrieval of memory due to the exposure to clothianidin. It was concluded that an acute exposure to clothianidin has an adverse effect on memory processing in honey bees.
[Léa Tison, Alexander Rößner, Susan Gerschewski, Randolf Menzel, The neonicotinoid clothianidin impairs memory processing in honey bees, Ecotoxicology and Environmental Safety, Volume 180, 2019, Pages 139-145, ISSN 0147-6513, https://doi.org/10.1016/j.ecoenv.2019.05.007.]
Bee pollination is economically and ecologically vital and recent declines in bee populations are therefore a concern. One possible cause of bee declines is pesticide use. Bumblebees exposed to imidacloprid, a neonicotinoid pesticide, have been shown to be less efficient foragers and collect less pollen on foraging trips than unexposed bees. We investigated whether bumblebees (Bombus impatiens) chronically exposed to imidacloprid at field-realistic levels of 2.6 and 10 ppb showed learning deficits that could affect foraging. Bumblebees were tested for their ability to associate flower colour with reward value in a simulated foraging environment. Bumblebees completed 10 foraging trips in which they collected sucrose solution from artificial flowers that varied in sucrose concentration. The reward quality of each artificial flower was predicted by corolla colour. Unexposed bumblebees acquired a preference for feeding on the most rewarding flower colour on the second foraging trip, while bumblebees exposed at 2.6 and 10 ppb did not until their third and fifth trip, respectively. The delay in preference acquisition in exposed bumblebees may be due to reduced flower sampling and shorter foraging trips. These results show that bumblebees exposed to imidacloprid are slow to learn the reward value of flowers and this may explain previously observed foraging inefficiencies associated with pesticide exposure.
[Phelps, J.D., Strang, C.G., Gbylik-Sikorska, M. et al. Imidacloprid slows the development of preference for rewarding food sources in bumblebees (Bombus impatiens). Ecotoxicology 27, 175–187 (2018). https://doi.org/10.1007/s10646-017-1883-3]
Neonicotinoids are the most widespread insecticides in agriculture, preferred for their low toxicity to mammals and their systemic nature. Nevertheless, there have been increasing concerns regarding their impact on non-target organisms. Glyphosate is also widely used in crops and, therefore, traces of this pesticide are likely to be found together with neonicotinoids. Although glyphosate is considered a herbicide, adverse effects have been found on animal species, including honey bees. Apis mellifera is one of the most important pollinators in agroecosystems and is exposed to both these pesticides. Traces can be found in nectar and pollen of flowers that honey bees visit, but also in honey stores inside the hive. Young workers, which perform in-hive tasks that are crucial for colony maintenance, are potentially exposed to both these contaminated resources. These workers present high plasticity and are susceptible to stimuli that can modulate their behaviour and impact on colony state. Therefore, by performing standardised assays to study sublethal effects of these pesticides, these bees can be used as bioindicators. We studied the effect of chronic joint exposure to field-realistic concentrations of the neonicotinoid imidacloprid and glyphosate on gustatory perception and olfactory learning. Both pesticides reduced sucrose responsiveness and had a negative effect on olfactory learning. Glyphosate also reduced food uptake during rearing. The results indicate differential susceptibility according to honey bee age. The two agrochemicals had adverse effects on different aspects of honey bee appetitive behaviour, which could have repercussions for food distribution, propagation of olfactory information and task coordination within the nest.
[Carolina Mengoni Goñalons, Walter M. Farina; Impaired associative learning after chronic exposure to pesticides in young adult honey bees. J Exp Biol 1 April 2018; 221 (7): jeb176644. doi: https://doi.org/10.1242/jeb.176644]
Queen health is crucial to colony survival of honeybees, since reproduction and colony growth rely solely on the queen. Queen failure is considered a relevant cause of colony losses, yet few data exist concerning effects of environmental stressors on queens. Here we demonstrate for the first time that exposure to field-realistic concentrations of neonicotinoid pesticides can severely affect the immunocompetence of queens of western honeybees (Apis mellifera L.). In young queens exposed to thiacloprid (200 µg/l or 2000 µg/l) or clothianidin (10 µg/l or 50 µg/l), the total hemocyte number and the proportion of active, differentiated hemocytes was significantly reduced. Moreover, functional aspects of the immune defence namely the wound healing/melanisation response, as well as the antimicrobial activity of the hemolymph were impaired. Our results demonstrate that neonicotinoid insecticides can negatively affect the immunocompetence of queens, possibly leading to an impaired disease resistance capacity.
[Brandt, A. et al. (2017) Immunosuppression in honeybee queens by the neonicotinoids Thiacloprid and Clothianidin, Scientific Reports. Available at: https://pubmed.ncbi.nlm.nih.gov/28680118/. ]
Learning and memory are crucial functions which enable insect pollinators to efficiently locate and extract floral rewards. Exposure to pesticides or infection by parasites may cause subtle but ecologically important changes in cognitive functions of pollinators. The potential interactive effects of these stressors on learning and memory have not yet been explored. Furthermore, sensitivity to stressors may differ between species, but few studies have compared responses in different species. Here, we show that chronic exposure to field-realistic levels of the neonicotinoid clothianidin impaired olfactory learning acquisition in honeybees, leading to potential impacts on colony fitness, but not in bumblebees. Infection by the microsporidian parasite Nosema ceranae slightly impaired learning in honeybees, but no interactive effects were observed. Nosema did not infect bumblebees (3% infection success). Nevertheless, Nosema-treated bumblebees had a slightly lower rate of learning than controls, but faster learning in combination with neonicotinoid exposure. This highlights the potential for complex interactive effects of stressors on learning. Our results underline that one cannot readily extrapolate findings from one bee species to others. This has important implications for regulatory risk assessments which generally use honeybees as a model for all bees.
[Piiroinen Saija and Goulson Dave 2016. Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebeesProc. R. Soc. B.28320160246 http://doi.org/10.1098/rspb.2016.0246]
It has been reported that the decimation of honey bees was because of pesticides of imidacloprid. The imidacloprid is a wildly used neonicotinoid insecticide. However, whether imidacloprid toxicity interferes with the spatial memory of echolocation bats is still unclear. Thus, we compared the spatial memory of Formosan leaf-nosed bats, Hipposideros terasensis, before and after chronic treatment with a low dose of imidacloprid. We observed that stereotyped flight patterns of echolocation bats that received chronic imidacloprid treatment were quite different from their originally learned paths. We further found that neural apoptosis in hippocampal CA1 and medial entorhinal cortex areas of echolocation bats that received imidacloprid treatment was significantly enhanced in comparison with echolocation bats that received sham treatment. Thus, we suggest that imidacloprid toxicity may interfere with the spatial memory of echolocation bats through neural apoptosis in hippocampal CA1 and medial entorhinal cortex areas. The results provide direct evidence that pesticide toxicity causes a spatial memory disorder in echolocation bats. This implies that agricultural pesticides may pose severe threats to the survival of echolocation bats.
[Hsiao, Chun-Jen; Lin, Ching-Lung; Lin, Tian-Yu; Wang, Sheue-Er; Wu, Chung-Hsin. Imidacloprid toxicity impairs spatial memory of echolocation bats through neural apoptosis in hippocampal CA1 and medial entorhinal cortex areas. NeuroReport 27(6):p 462-468, April 13, 2016. | DOI: 10.1097/WNR.0000000000000562]
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. ]
Chlorpyrifos is an organophosphate pesticide used around the world to protect food crops against insects and mites. Despite guidelines for chlorpyrifos usage, including precautions to protect beneficial insects, such as honeybees from spray drift, this pesticide has been detected in bees in various countries, indicating that exposure still occurs. Here, we examined chlorpyrifos levels in bees collected from 17 locations in Otago, New Zealand, and compared doses of this pesticide that cause sub-lethal effects on learning performance under laboratory conditions with amounts of chlorpyrifos detected in the bees in the field. The pesticide was detected at 17 % of the sites sampled and in 12 % of the colonies examined. Amounts detected ranged from 35 to 286 pg.bee−1, far below the LD50 of ~100 ng.bee−1. We detected no adverse effect of chlorpyrifos on aversive learning, but the formation and retrieval of appetitive olfactory memories was severely affected. Chlorpyrifos fed to bees in amounts several orders of magnitude lower than the LD50, and also lower than levels detected in bees, was found to slow appetitive learning and reduce the specificity of memory recall. As learning and memory play a central role in the behavioral ecology and communication of foraging bees, chlorpyrifos, even in sublethal doses, may threaten the success and survival of this important insect pollinator.
[Urlacher, E., Monchanin, C., Rivière, C. et al. Measurements of Chlorpyrifos Levels in Forager Bees and Comparison with Levels that Disrupt Honey Bee Odor-Mediated Learning Under Laboratory Conditions. J Chem Ecol 42, 127–138 (2016). https://doi.org/10.1007/s10886-016-0672-4]
Xenobiotics such as the neonicotinoid pesticide, imidacloprid, are used globally, but their effects on native bee species are poorly understood. We studied the effects of sublethal doses of imidacloprid on olfactory learning in the native honey bee species, Apis cerana, an important pollinator of agricultural and native plants throughout Asia. We provide the first evidence that imidacloprid can impair learning in A. cerana workers exposed as adults or as larvae. Adults that ingested a single imidacloprid dose as low as 0.1 ng/bee had significantly reduced olfactory learning acquisition, which was 1.6-fold higher in control bees. Longer-term learning (1-17 h after the last learning trial) was also impaired. Bees exposed as larvae to a total dose of 0.24 ng/bee did not have reduced survival to adulthood. However, these larval-treated bees had significantly impaired olfactory learning when tested as adults: control bees exhibited up to 4.8-fold better short-term learning acquisition, though longer-term learning was not affected. Thus, sublethal cognitive deficits elicited by neonicotinoids on a broad range of native bee species deserve further study.
[Tan, K., Chen, W., Dong, S. et al. A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Sci Rep 5, 10989 (2015). https://doi.org/10.1038/srep10989]
Bumblebees are exposed to pesticides applied for crop protection while foraging on treated plants, with increasing evidence suggesting that this sublethal exposure has implications for pollinator declines. The challenges of navigating and learning to manipulate many different flowers underline the critical role learning plays for the foraging success and survival of bees. We assessed the impacts of both acute and chronic exposure to field-realistic levels of a widely applied neonicotinoid insecticide, thiamethoxam, on bumblebee odour learning and memory. Although bees exposed to acute doses showed conditioned responses less frequently than controls, we found no difference in the number of individuals able to learn at field-realistic exposure levels. However, following chronic pesticide exposure, bees exposed to field-realistic levels learnt more slowly and their short-term memory was significantly impaired following exposure to 2.4 ppb pesticide. These results indicate that field-realistic pesticide exposure can have appreciable impacts on learning and memory, with potential implications for essential individual behaviour and colony fitness.
[Stanley, D., Smith, K. & Raine, N. Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide. Sci Rep 5, 16508 (2015). https://doi.org/10.1038/srep16508]
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. ]