Impaired associative learning after chronic exposure to pesticides in young adult honey bees

Goñalons, Carolina Mengoni; Farina, Walter M.

doi:10.1242/jeb.176644

Cited by 61 publications

(47 citation statements)

References 52 publications

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“…3% w/v) but not with high concentrations (e.g. 30% w/v; Aliouane et al, 2009 ; Demares et al, 2018 ; Eiri and Nieh, 2016 ; Mengoni Goñalons and Farina, 2015 , 2018 ). Based on these published studies, we expected that perception of the unconditioned stimuli in our experiments would not be affected by neonicotinoid exposure, as we used very concentrated sucrose as one of our unconditioned stimuli (34% w/v sucrose).…”

Section: Discussionmentioning

confidence: 88%

“…Bumblebees fed an acute dose of IMD prior to a task had difficulty learning to distinguish artificial flowers with different scents ( Muth and Leonard, 2019 ). Young worker honeybees between 5 and 14 days old exposed to IMD over longer periods (5–14 days) had slower rates of learning in both simple and differential learning tasks ( Mengoni Goñalons and Farina, 2018 ). Others have found that IMD at a similar dose reduces the rate of acquisition during aversive learning using cues mimicking a predatory attack ( Tan et al, 2014 ; Zhang and Nieh, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

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Honeybees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide

Mustard

Gott

Scott

et al. 2020

Journal of Experimental Biology

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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.

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Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Honeybees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide

Mustard

Gott

Scott

et al. 2020

Journal of Experimental Biology

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“…We found that, under laboratory conditions and without pathogen challenge, only the higher doses of glyphosate (0.1 mM and 1.0 mM) reduced the life span of young worker bees. In studies that did not examine the role of gut microbiota, glyphosate was shown to directly compromise larval development and adult behavior (12,(42)(43)(44)(45), although some other studies failed to detect effects on survivorship (20,46,47). Tylosin, which had large effects on the gut microbiota, increased mortality in only one of the four trials with caged laboratory bees (Fig.…”

Section: Discussionmentioning

confidence: 99%

Impact of Glyphosate on the Honey Bee Gut Microbiota: Effects of Intensity, Duration, and Timing of Exposure

Motta

Moran

2020

mSystems

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Exposure to anthropogenic chemicals may indirectly compromise animal health by perturbing the gut microbiota. For example, the widely used herbicide glyphosate can affect the microbiota of honey bees, reducing the abundance of beneficial bacterial species that contribute to immune regulation and pathogen resistance. Previous studies have not addressed how this impact depends on concentration, duration of exposure, or stage of microbiota establishment. Worker bees acquire their microbiota from nestmates early in adult life, when they can also be exposed to chemicals collected by foragers or added to the hives. Here, we investigated how the gut microbiota of honey bees is affected by different concentrations of glyphosate and compared the effects with those caused by tylosin, an antibiotic commonly used to treat hives. We treated newly emerged workers at the stage at which they acquire the microbiota and also workers with established gut microbiota. Treatments consisted of exposure to sucrose syrup containing glyphosate in concentrations ranging from 0.01 mM to 1.0 mM or tylosin at 0.1 mM. Based on 16S rRNA amplicon sequencing and quantitative PCR (qPCR) determination of abundances, glyphosate perturbed the gut microbiota of honey bees regardless of age or period of exposure. Snodgrassella alvi was the most affected bacterial species and responded to glyphosate in a dose-dependent way. Tylosin also perturbed the microbiota, especially at the stage of acquisition, and the effects differed sharply from the effects of glyphosate. These findings show that sublethal doses of glyphosate (0.04 to 1.0 mM) and tylosin (0.1 mM) affect the microbiota of honey bees. IMPORTANCE As is true of many animal species, honey bees depend on their gut microbiota for health. The bee gut microbiota has been shown to regulate the host immune system and to protect against pathogenic diseases, and disruption of the normal microbiota leads to increased mortality. Understanding these effects can give broad insights into vulnerabilities of gut communities, and, in the case of honey bees, could provide information useful for promoting the health of these economically critical insects, which provide us with crop pollination services as well as honey and other products. The bee gut microbiota is acquired early in adult life and can be compromised by antibiotics and other chemicals. The globally used weed killer glyphosate was previously found to impact the gut microbiota of honey bees following sustained exposure. In the present study, we address how this impact depends on concentration, duration of exposure, and stage of community establishment. We found that sublethal doses of glyphosate reduce the abundance of beneficial bacteria and affect microbial diversity in the guts of honey bees, regardless of whether exposure occurs during or after microbiota acquisition. We also compared the effects of glyphosate to those of tylosin, an antibiotic used in beekeeping, and observed that tylosin effects diverge from those caused by glyphosate and are greater during microbiota acquisition. Such perturbations are not immediately lethal to bees but, depending on exposure level, can decrease survivorship under laboratory conditions.

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“…In the honeybee, glyphosate or Roundup formulation can induce an increase in lipid peroxidation, a decrease in β-carotene and derived antioxidants, and a reduction in acetylcholine esterase activity [13,19–21]. A chronic exposure to the herbicide can reduce the honeybee learning performance while acute exposure was shown to reduce its short-term memory [22,23]. Glyphosate can also affect the honeybee navigation by increasing the time and path of homeward flight [24].…”

Section: Introductionmentioning

confidence: 99%

Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota

et al. 2019

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The honeybee ( Apis mellifera ) has to cope with multiple environmental stressors, especially pesticides. Among those, the herbicide glyphosate and its main metabolite, the aminomethylphosphonic acid (AMPA), are among the most abundant and ubiquitous contaminant in the environment. Through the foraging and storing of contaminated resources, honeybees are exposed to these xenobiotics. As ingested glyphosate and AMPA are directly in contact with the honeybee gut microbiota, we used quantitative PCR to test whether they could induce significant changes in the relative abundance of the major gut bacterial taxa. Glyphosate induced a strong decrease in Snodgrassella alvi , a partial decrease of a Gilliamella apicola and an increase in Lactobacillus spp. abundances. In vitro , glyphosate reduced the growth of S . alvi and G . apicola but not Lactobacillus kunkeei . Although being no bee killer, we confirmed that glyphosate can have sublethal effects on the honeybee microbiota. To test whether such imbalanced microbiota could favor pathogen development, honeybees were exposed to glyphosate and to spores of the intestinal parasite Nosema ceranae . Glyphosate did not significantly enhance the effect of the parasite infection. Concerning AMPA, while it could reduce the growth of G . apicola in vitro , it did not induce any significant change in the honeybee microbiota, suggesting that glyphosate is the active component modifying the gut communities.

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Impaired associative learning after chronic exposure to pesticides in young adult honey bees

Cited by 61 publications

References 52 publications

Honeybees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide

Honeybees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide

Impact of Glyphosate on the Honey Bee Gut Microbiota: Effects of Intensity, Duration, and Timing of Exposure

Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota

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