A common fungicide, Pristine®, impairs olfactory associative learning performance in honey bees (Apis mellifera)

DesJardins, Nicole; Fisher, Adrian; Öztürk, Cahit; Fewell, Jennifer H.; DeGrandi-Hoffman, Gloria; Harrison, Jon F.; Smith, Brian H.

doi:10.1016/j.envpol.2021.117720

Cited by 30 publications

(14 citation statements)

References 68 publications

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“…As Pristine is able to pass through the gut and into the hemolymph [64], it is plausible that it could also pass through the sheath surrounding the brain and poison mitochondria. This explanation goes along with our previous finding that Pristine impairs olfactory associative learning performance [45], which provides a basic measurement of a bee's ability to learn about relevant environmental stimuli, a necessary ability for successful homing. Likewise, royalsocietypublishing.org/journal/rspb Proc.…”

Section: Discussionsupporting

confidence: 69%

See 1 more Smart Citation

Synergistic negative effects between a fungicide and high temperatures on homing behaviours in honeybees

DesJardins,

Chester,

Ozturk

et al. 2024

Proc. R. Soc. B.

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Interactions between environmental stressors may contribute to ongoing pollinator declines, but have not been extensively studied. Here, we examined the interaction between the agricultural fungicide Pristine (active ingredients: 25.2% boscalid, 12.8% pyraclostrobin) and high temperatures on critical honeybee behaviours. We have previously shown that consumption of field-realistic levels of this fungicide shortens worker lifespan in the field and impairs associative learning performance in a laboratory-based assay. We hypothesized that Pristine would also impair homing and foraging behaviours in the field, and that an interaction with hot weather would exacerbate this effect. Both field-relevant Pristine exposure and higher air temperatures reduced the probability of successful return on their own. Together, the two factors synergistically reduced the probability of return and increased the time required for bees to return to the hive. Pristine did not affect the masses of pollen or volumes of nectar or water brought back to the hive by foragers, and it did not affect the ratio of forager types in a colony. However, Pristine-fed bees brought more concentrated nectar back to the hive. As both agrochemical usage and heat waves increase, additive and synergistic negative effects may pose major threats to pollinators and sustainable agriculture.

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Section: Discussionsupporting

confidence: 69%

“…We have previously shown that the fungicide Pristine impairs olfactory associative learning performance in honeybees [45]. We therefore hypothesized that it would negatively impact homing and foraging behaviours, which depend on the bee's learning ability.…”

Section: Introductionmentioning

confidence: 99%

Synergistic negative effects between a fungicide and high temperatures on homing behaviours in honeybees

DesJardins,

Chester,

Ozturk

et al. 2024

Proc. R. Soc. B.

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“…Sublethal impacts can be anticipated for many other AIs identified in our study. For instance, there is evidence that exposure to the fungicide Pristine, which is a combination of pyraclostrobin and boscalid, can inhibit mitochondrial function 72 , impair olfactory learning 73 , and reduce honey bee worker lifespan and colony population size 74 . This fungicide is used in blueberry fields during bloom to combat diseases and was detected in over 90% of bee collected pollen, over 75% of wax, over 50% of whole bees, and over 30% of flowers.…”

Section: Discussionmentioning

confidence: 99%

Pesticide risk to managed bees during blueberry pollination is primarily driven by off-farm exposures

Graham

Milbrath

Zhang

et al. 2022

Sci Rep

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When managed bee colonies are brought to farms for crop pollination, they can be exposed to pesticide residues. Quantifying the risk posed by these exposures can indicate which pesticides are of the greatest concern and helps focus efforts to reduce the most harmful exposures. To estimate the risk from pesticides to bees while they are pollinating blueberry fields, we sampled blueberry flowers, foraging bees, pollen collected by returning honey bee and bumble bee foragers at colonies, and wax from honey bee hives in blooming blueberry farms in southwest Michigan. We screened the samples for 261 active ingredients using a modified QuEChERS method. The most abundant pesticides were those applied by blueberry growers during blueberry bloom (e.g., fenbuconazole and methoxyfenozide). However, we also detected highly toxic pesticides not used in this crop during bloom (or other times of the season) including the insecticides chlorpyrifos, clothianidin, avermectin, thiamethoxam, and imidacloprid. Using LD50 values for contact and oral exposure to honey bees and bumble bees, we calculated the Risk Quotient (RQ) for each individual pesticide and the average sample RQ for each farm. RQ values were considered in relation to the U.S. Environmental Protection Agency acute contact level of concern (LOC, 0.4), the European Food Safety Authority (EFSA) acute contact LOC (0.2) and the EFSA chronic oral LOC (0.03). Pollen samples were most likely to exceed LOC values, with the percent of samples above EFSA’s chronic oral LOC being 0% for flowers, 3.4% for whole honey bees, 0% for whole bumble bees, 72.4% for honey bee pollen in 2018, 45.4% of honey bee pollen in 2019, 46.7% of bumble bee pollen in 2019, and 3.5% of honey bee wax samples. Average pollen sample RQ values were above the EFSA chronic LOC in 92.9% of farms in 2018 and 42.9% of farms in 2019 for honey bee collected pollen, and 46.7% of farms for bumble bee collected pollen in 2019. Landscape analyses indicated that sample RQ was positively correlated with the abundance of apple and cherry orchards located within the flight range of the bees, though this varied between bee species and landscape scale. There was no correlation with abundance of blueberry production. Our results highlight the need to mitigate pesticide risk to bees across agricultural landscapes, in addition to focusing on the impact of applications on the farms where they are applied.

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“…The benomyl stress (5 g/kg) led to a total of 5,759 DEGs being upregulated in the worker bees of A. mellifera , and most of the DEGs were involved in the functions of immunity, detoxification, biological metabolism, and regulation, such as light conduction, MAPK, calcium ion pathway and other 12 pathways ( Dai et al, 2021 ). DesJardins et al (2021) found the compound fungicides Pristine ® showed significant sublethal effects on the learning performance of A. mellifera and lead the work type conversion of nurse bee to forage bee.…”

Section: Introductionmentioning

confidence: 98%

Field recommended concentrations of pyraclostrobin exposure disturb the development and immune response of worker bees (Apis mellifera L.) larvae and pupae

Xiong

Gan²,

Wang³

et al. 2023

Front. Physiol.

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The strobilurin fungicide pyraclostrobin is widely used to prevent and control the fungal diseases of various nectar and pollen plants. Honeybees also directly or indirectly contact this fungicide with a long-term exposure period. However, the effects of pyraclostrobin on the development and physiology of Apis mellifera larvae and pupae during continuous exposure have been rarely known. To investigate the effects of field-realistic concentrations of pyraclostrobin on honeybee survival and development, the 2-day-old larvae were continuously fed with different pyraclostrobin solutions (100 mg/L and 83.3 mg/L), and the expression of development-, nutrient-, and immune-related genes in larvae and pupae were examined. The results showed that two field-realistic concentrations of pyraclostrobin (100 and 83.3 mg/L) significantly decreased the survival and capped rate of larvae, the weight of pupae and newly emerged adults, and such decrease was a positive correlation to the treatment concentrations. qPCR results showed that pyraclostrobin could induce the expression of Usp, ILP2, Vg, Defensin1, and Hymenoptaecin, decrease the expression of Hex100, Apidaecin, and Abaecin in larvae, could increase the expression of Ecr, Usp, Hex70b, Vg, Apidaecin, and Hymenoptaecin, and decreased the expression of ILP1, Hex100 and Defensin1in pupae. These results reflect pyraclostrobin could decrease nutrient metabolism, immune competence and seriously affect the development of honeybees. It should be used cautiously in agricultural practices, especially in the process of bee pollination.

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A common fungicide, Pristine®, impairs olfactory associative learning performance in honey bees (Apis mellifera)

Cited by 30 publications

References 68 publications

Synergistic negative effects between a fungicide and high temperatures on homing behaviours in honeybees

Synergistic negative effects between a fungicide and high temperatures on homing behaviours in honeybees

Pesticide risk to managed bees during blueberry pollination is primarily driven by off-farm exposures

Field recommended concentrations of pyraclostrobin exposure disturb the development and immune response of worker bees (Apis mellifera L.) larvae and pupae

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