The global challenge to increase agricultural production goes along with the need of decreasing pesticide risks. The European Union (EU) therefore evaluates and controls the risks posed by pesticides by regulating their authorisation... more
The global challenge to increase agricultural production goes along with the need of decreasing pesticide risks. The European Union (EU) therefore evaluates and controls the risks posed by pesticides by regulating their authorisation through the science-based Risk Assessment process. Member States can however act in derogation to this process and grant the Emergency Authorisation (EA) of pesticides that are currently non-authorised. To protect the health of humans and the environment, Emergency Authorisations are only permitted in exceptional circumstances of agricultural emergency: their use should be limited (i.e., cannot exceed 120 days and one growing season) and concurrent research on alternative strategies must be enforced. Here, we assessed the impact of the Emergency Authorisations process to human and environmental health. Bees, bioindicators of environmental health, were used as model species. Our research demonstrates that i) Emergency Authorisations are widely used throughout EU Member States (annually granted Emergency Authorisations(min-max, 2017–2021) = 593–660); ii) 12 % of Emergency Authorisations granted the use of pesticides for longer than prescribed by EU regulations; iii) 37 % of Emergency Authorisations were repeatedly granted over time by the same Member State for the same agricultural purpose (i.e., to control the same pest on the same crop); iv) 21 % of Emergency Authorisations granted the use of Active Substances non-approved by risk assessment (EA-ASs Type3) which consequently contaminate the environment (44 % of environmental biomonitoring studies found EA-AS Type3) while being significantly more toxic to pollinators than regularly approved ASs. To facilitate the implementation of sustainable control strategies towards a safer environment for humans and other animals, we identified the most frequent agricultural emergencies and the key research needs. This first quantitative assessment of the Emergency Authorisation process unveils an enduring state of agricultural emergency that acts in derogation of the EU Regulation, leading to broad human, animal, and environmental implications.
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Flupyradifurone (FPF, Sivanto®) is a new butenolide insecticide that, like the neonicotinoids, is a systemic nicotinic acetylcholine agonist (nAChR). However, FPF is considered bee-safe (according to standard Risk Assessment tests), and... more
Flupyradifurone (FPF, Sivanto®) is a new butenolide insecticide that, like the neonicotinoids, is a systemic nicotinic acetylcholine agonist (nAChR). However, FPF is considered bee-safe (according to standard Risk Assessment tests), and thus a potential solution to the adverse effects of other pesticides on beneficial insects. To date, no studies have examined the impact of nutritional stress (decreased food diversity and quality) and FPF exposure on bee health although both stressors can occur, especially around agricultural monocultures. We therefore tested the effects of a field-realistic FPF concentration (4 ppm, FPFdaily dose = 241 ± 4 ng/bee/day, 1/12 of LD50) and nutritional stress (nectar with low-sugar concentrations) on honey bee (Apis mellifera L.) mortality, food consumption, thermoregulation, flight success (unsuccessful vs. successful), and flight ability (duration, distance, velocity). Flight and thermoregulation are critical to colony health: bees fly to collect food and reproduce, and they thermoregulate to increase flight efficiency and to rear brood. We studied the effects across seasons because seasonality can influence bee sensitivity to environmental stress. We demonstrate that, depending upon season and nutritional stress, FPF can reduce bee survival (-14%), food consumption (-14%), thermoregulation (-4%, i.e. hypothermia), flight success (-19%), and increase flight velocity (+13%). Because pesticide exposure and nutritional stress can co-occur, we suggest that future studies and pesticide risk assessments consider both seasonality and nutritional stress when evaluating pesticide safety for bees.
Research Interests: Food Safety, Thermoregulation, Nutrition, Animal Behavior, Environmental Toxicology, and 15 moreToxicology, Food and Nutrition, Risk assessment, Environmental Risk Assesment, Animal Nutrition, Survival, Bees, Food Consumption, Pesticides, Synergy, Honey Bees, Survival Rate, Sublethal, Combinations, and Animal Flight
The honeybee (Apis mellifera L.) is an important pollinator and a model for pesticide effects on insect pollinators. The effects of agricultural pesticides on honeybee health have therefore raised concern. Bees can be exposed to multiple... more
The honeybee (Apis mellifera L.) is an important pollinator and a model for pesticide effects on insect pollinators. The effects of agricultural pesticides on honeybee health have therefore raised concern. Bees can be exposed to multiple pesticides that may interact synergistically, amplifying their side effects. Attention has focused on neonicotinoid pesticides, but flupyradifur-one (FPF) is a novel butenolide insecticide that is also systemic and a nicotinic acetylcholine receptor (nAChR) agonist. We therefore tested the lethal and sublethal toxic effects of FPF over different seasons and worker types, and the interaction of FPF with a common SBI fungicide, propicona-zole. We provide the first demonstration of adverse synergistic effects on bee survival and behaviour (poor coordination, hyperactivity, apathy) even at FPF field-realistic doses (worst-case scenarios). Pesticide effects were significantly influenced by worker type and season. Foragers were consistently more susceptible to the pesticides (4-fold greater effect) than in-hive bees, and both worker types were more strongly affected by FPF in summer as compared with spring. Because risk assessment (RA) requires relatively limited tests that only marginally address bee behaviour and do not consider the influence of bee age and season, our results raise concerns about the safety of approved pesticides, including FPF. We suggest that pesticide RA also test for common chemical mixture synergies on behaviour and survival.
Research Interests: Animal Behavior, Interaction, Pesticide ecotoxicology, Pesticide Residues, Beekeeping, and 14 moreInsecticides, Survival, Pesticide, Fungicides, Pesticides, Pesticides Risk assessment, Synergy, Honey Bees, Abnormal Behavior, Neonicotinoid, Synergism, Sublethal doses, Neonicotinoid Pesticides, and Neonicotinoids
Honey bees provide key ecosystem services. To pollinate and to sustain the colony, workers must walk, climb, and use phototaxis as they move inside and outside the nest. Phototaxis, orientation to light, is linked to sucrose... more
Honey bees provide key ecosystem services. To pollinate and to sustain the colony, workers must walk, climb, and use phototaxis as they move inside and outside the nest. Phototaxis, orientation to light, is linked to sucrose responsiveness and the transition of work from inside to outside the nest, and is also a key component of division of labour. However, the sublethal effects of pesticides on locomotion and movement to light are relatively poorly understood. Thiamethoxam (TMX) is a common neonicotinoid pesticide that bees can consume in nectar and pollen. We used a vertical arena illuminated from the top to test the effects of acute and chronic sublethal exposures to TMX. Acute consumption (1.34 ng/bee) impaired locomotion, caused hyperactivity (velocity: +109%; time moving: +44%) shortly after exposure (30 min), and impaired motor functions (falls: +83%; time top: −43%; time bottom: +93%; abnormal behaviours: +138%; inability to ascend: +280%) over a longer period (60 min). A 2-day chronic exposure (field-relevant daily intakes of 1.42–3.48 ng/bee/day) impaired bee ability to ascend. TMX increased movement to light after acute and chronic exposure. Thus, TMX could reduce colony health by harming worker locomotion and, potentially, alter division of labour if bees move outside or remain outdoors.
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The honey bee is a major pollinator whose health is of global concern. Declines in bee health are related to multiple factors, including resource quality and pesticide contamination. Intensive agricultural areas with crop monocultures... more
The honey bee is a major pollinator whose health is of global concern. Declines in bee health are related to multiple factors, including resource quality and pesticide contamination. Intensive agricultural areas with crop monocultures potentially reduce the quality and quantity of available nutrients and expose bee foragers to pesticides. However, there is, to date, no evidence for syner-gistic effects between pesticides and nutritional stress in animals. The neonicotinoids clothianidin (CLO) and thiamethoxam (TMX) are common systemic pesticides that are used worldwide and found in nectar and pollen. We therefore tested if nutritional stress (limited access to nectar and access to nectar with low-sugar concentrations) and sublethal, field-realistic acute exposures to two neonicotinoids (CLO and TMX at 1/5 and 1/25 of LD 50) could alter bee survival, food consumption and haemolymph sugar levels. Bee survival was synergistically reduced by the combination of poor nutrition and pesticide exposure (250%). Nutritional and pesticide stressors reduced also food consumption (248%) and haemolymph levels of glucose (260%) and trehalose (227%). Our results provide the first demonstration that field-realistic nutritional stress and pesticide exposure can synergistically interact and cause significant harm to animal survival. These findings have implications for current pesticide risk assessment and pollinator protection.
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Honey bee (Apis mellifera L.) health is compromised by complex interactions between multiple stressors, among which pesticides play a major role. To better understand the extent of honey bee colonies' exposure to pesticides in time and... more
Honey bee (Apis mellifera L.) health is compromised by complex interactions between multiple stressors, among which pesticides play a major role. To better understand the extent of honey bee colonies' exposure to pesticides in time and space, we conducted a survey by collecting corbicular pollen from returning honey bee foragers in 53 Italian apiaries during the active beekeeping season of 3 subsequent years (2012–2014). Of 554 pollen samples analysed for pesticide residues, 62% contained at least one pesticide. The overall rate of multiresidual samples (38%) was higher than the rate of single pesticide samples (24%), reaching a maximum of 7 pesticides per sample (1%). Over 3years, 18 different pesticides were detected (10 fungicides and 8 insecticides) out of 66 analysed. Pesticide concentrations reached the level of concern for bee health (Hazard Quotient (HQ) higher than 1000) at least once in 13% of the apiaries and exceeded the thresholds of safety for human dietary intake (Acute Reference Dose (ARfD), the Acceptable Daily Intake (ADI), and the Maximum Residue Limit (MRL)) in 39% of the analysis. The pesticide which was most frequently detected was the insecticide chlorpyrifos (30% of the samples overall, exceeding ARfD, ADI, or MRL in 99% of the positive ones), followed by the fungicides mandipropamid (19%), metalaxyl (16%), spiroxamine (15%), and the neonicotinoid insecticide imidacloprid (12%). Imidacloprid had also the highest HQ level (5054, with 12% of its positive samples with HQ higher than 1000). This 3year survey provides further insights on the contamination caused by agricultural pesticide use on honey bee colonies. Bee-collected pollen is shown to be a valuable tool for environmental monitoring, and for the detection of illegal uses of pesticides.
Research Interests: Entomology, Organic agriculture, Toxicology, Environmental Management, Risk assessment, and 12 morePesticide ecotoxicology, Beekeeping, Bees, Pollen, Pesticides, Bees Health, Honey Bees, Human health, entomology (HONEYBEE/STINGLESS BEE HEALTH AND NUTRITION), Neonicotinoid, Chlorpyrifos, and Farming Practices
Pesticides can pose environmental risks, and a common neonicotinoid pesticide, thiamethoxam, decreases homing success in honey bees. Neonicotinoids can alter bee navigation, but we present the first evidence that neonicotinoid exposure... more
Pesticides can pose environmental risks, and a common neonicotinoid pesticide, thiamethoxam, decreases homing success in honey bees. Neonicotinoids can alter bee navigation, but we present the first evidence that neonicotinoid exposure alone can impair the physical ability of bees to fly. We tested the effects of acute or chronic exposure to thiamethoxam on the flight ability of foragers in flight mills. Within 1 h of consuming a single sublethal dose (1.34 ng/bee), foragers showed excitation and significantly increased flight duration (+78%) and distance (+72%). Chronic exposure significantly decreased flight duration (-54%), distance (-56%), and average velocity (-7%) after either one or two days of continuous exposure that resulted in bees ingesting field-relevant thiamethoxam daily doses of 1.96-2.90 ng/bee/day. These results provide the first demonstration that acute or chronic exposure to a neonicotinoid alone can significantly alter bee flight. Such exposure may impair foraging and homing, which are vital to normal colony function and ecosystem services.
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Thiamethoxam is a widely used neonicotinoid pesticide that, as agonist of the nicotinic acetylcholine receptors, has been shown to elicit a variety of sublethal effects in honey bees. However, information concerning neonicotinoid effects... more
Thiamethoxam is a widely used neonicotinoid pesticide that, as agonist of the nicotinic acetylcholine receptors, has been shown to elicit a variety of sublethal effects in honey bees. However, information concerning neonicotinoid effects on honey bee thermoregulation is lacking. Thermoregulation is an essential ability for the honey bee that guarantees the success of foraging and many in-hive tasks, especially brood rearing. We tested the effects of acute exposure to thiamethoxam (0.2, 1, 2 ng/bee) on the thorax temperatures of foragers exposed to low (22 °C) and high (33 °C) temperature environments. Thiamethoxam significantly altered honey bee thorax temperature at all doses tested; the effects elicited varied depending on the environmental temperature and pesticide dose to which individuals were exposed. When bees were exposed to the high temperature environment, the high dose of thiamethoxam increased their tho-rax temperature 1–2 h after exposure. When bees were exposed to the low temperature, the higher doses of the neonicotinoid reduced bee thorax temperatures 60–90 min after treatment. In both experiments, the neonicotinoid decreased the temperature of bees the day following the exposure. After a cold shock (5 min at 4 °C), the two higher doses elicited a decrease of the thorax temperature, while the lower dose caused an increase, compared to the control. These alterations in thermoregulation caused by thiamethoxam may affect bee foraging activity and a variety of in-hive tasks, likely leading to negative consequences at the colony level. Our results shed light on sublethal effect of pesticides which our bees have to deal with.
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The official guidelines for the assessment of the risk of pesticides on honeybees are based on specific protocols. They contain the procedures that must be applied in order to make the results usable for the pesticide registration... more
The official guidelines for the assessment of the risk of pesticides on honeybees are based on specific protocols. They contain the procedures that must be applied in order to make the results usable for the pesticide registration process. The described test ...