Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees

Almasri, Hanine; Tavares, Daiana Antonia; Pioz, Maryline; Sené, Déborah; Tchamitchian, Sylvie; Cousin, Marianne; Brunet, Jean-Luc; Belzunces, Luc

doi:10.1016/j.ecoenv.2020.111013

Cited by 77 publications

(62 citation statements)

References 93 publications

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“…Moreover, more than one pesticide is often used by farmers over a growing season. The chronic exposure to pesticides alone or in combination represents a threat for the honeybee populations (Calatayud-Vernich et al 2016 ; Gill et al 2012 ; Johnson et al 2013 ; Tosi et al 2018 ; Zhu et al 2014 ), altering their physiology through metabolism, immunity, the nervous system, detoxification, and antioxidant defenses (Almasri et al 2020 ). Pesticides can reach the hive by contaminated pollen collected by foraging honeybees.…”

Section: Discussionmentioning

confidence: 99%

First application of an Integrated Biological Response index to assess the ecotoxicological status of honeybees from rural and urban areas

Caliani

Campani

Conti

et al. 2021

Environ Sci Pollut Res

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Understanding the effects of environmental contaminants on honeybees is essential to minimize their impacts on these important pollinating insects. The aim of this study was to assess the ecotoxicological status of honeybees in environments undergoing different anthropic pressure: a wood (reference site), an orchard, an agricultural area, and an urban site, using a multi-biomarker approach. To synthetically represent the ecotoxicological status of the honeybees, the responses of the single biomarkers were integrated by the Integrated Biological Response (IBRv2) index. Overall, the strongest alteration of the ecotoxicological status (IBRv2 = 7.52) was detected in the bees from the orchard due to the alteration of metabolic and genotoxicity biomarkers indicating the presence of pesticides, metals, and lipophilic compounds. Honeybees from the cultivated area (IBRv2 = 7.18) revealed an alteration especially in neurotoxicity, metabolic, and genotoxicity biomarkers probably related to the presence of pesticides, especially fungicides. Finally, in the urban area (IBRv2 = 6.60), the biomarker results (GST, lysozyme, and hemocytes) indicated immunosuppression in the honeybees and the effects of the presence of lipophilic compounds and metals in the environment.

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Section: Discussionmentioning

confidence: 99%

First application of an Integrated Biological Response index to assess the ecotoxicological status of honeybees from rural and urban areas

Caliani

Campani

Conti

et al. 2021

Environ Sci Pollut Res

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“…In the EU, glyphosate did not meet the toxicity thresholds required to trigger higher tier testing, so was approved for use with only very minimal bee testing ( EFSA, 2015 ). Alongside regulatory testing a number of academic experiments have found that oral exposure to glyphosate does not cause mortality in adult bees ( Herbert et al, 2014 ; Gonalons & Farina, 2018 ; Motta, Raymann & Moran, 2018 ; Blot et al, 2019 ; Faita et al, 2020 ; Almasri et al, 2021 ), although there is mixed evidence, with Almasri et al (2020) and Motta & Moran (2020) finding mortality at doses considerably lower than doses found to be non-lethal in other work.…”

Section: Introductionmentioning

confidence: 99%

No evidence of effects or interaction between the widely used herbicide, glyphosate, and a common parasite in bumble bees

Straw

Brown

2021

PeerJ

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Background Glyphosate is the world’s most used pesticide and it is used without the mitigation measures that could reduce the exposure of pollinators to it. However, studies are starting to suggest negative impacts of this pesticide on bees, an essential group of pollinators. Accordingly, whether glyphosate, alone or alongside other stressors, is detrimental to bee health is a vital question. Bees are suffering declines across the globe, and pesticides, including glyphosate, have been suggested as being factors in these declines. Methods Here we test, across a range of experimental paradigms, whether glyphosate impacts a wild bumble bee species, Bombus terrestris. In addition, we build upon existing work with honey bees testing glyphosate-parasite interactions by conducting fully crossed experiments with glyphosate and a common bumble bee trypanosome gut parasite, Crithidia bombi. We utilised regulatory acute toxicity testing protocols, modified to allow for exposure to multiple stressors. These protocols are expanded upon to test for effects on long term survival (20 days). Microcolony testing, using unmated workers, was employed to measure the impacts of either stressor on a proxy of reproductive success. This microcolony testing was conducted with both acute and chronic exposure to cover a range of exposure scenarios. Results We found no effects of acute or chronic exposure to glyphosate, over a range of timespans post-exposure, on mortality or a range of sublethal metrics. We also found no interaction between glyphosate and Crithidia bombi in any metric, although there was conflicting evidence of increased parasite intensity after an acute exposure to glyphosate. In contrast to published literature, we found no direct impacts of this parasite on bee health. Our testing focussed on mortality and worker reproduction, so impacts of either or both of these stressors on other sublethal metrics could still exist. Conclusions Our results expand the current knowledge on glyphosate by testing a previously untested species, Bombus terrestris, using acute exposure, and by incorporating a parasite never before tested alongside glyphosate. In conclusion our results find that glyphosate, as an active ingredient, is unlikely to be harmful to bumble bees either alone, or alongside Crithidia bombi.

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“…In semi-field studies different responses both at macroscopic and microscopic levels were considered; however, in this review, only 14 papers of this kind were found. Honey bees, in the field, are exposed to multiple stressors and most of the field papers were monitoring studies where accumulation of various contaminants in Apis mellifera were investigated; only 8 papers [28,33,50,57,62,71,83,95] analysed the sublethal effects of the contaminant mixtures on Apis mellifera. All these studies highlighted that honey bees are sensitive bioindicators of environmental pollution.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, detoxification and antioxidant enzymes activities seem to be altered by neonicotinoids, such GST [53,81,82], CAT [53], PPO [84], ALP [53] and CYP450 [94] activities. Moreover, these compounds may affect the immune system for instance, by modulating the content of vitellogenin [47,101], by reducing the hemocytes density, encapsulation response and antimicrobial activity [83], and by modulating the relative abundance of several key gut microbial molecules [66]. Several authors studied the effects of pyrethroid insecticides, such as deltamethrin, bifenthrin, cypermethrin, permethrin, and λ-cyhalotrin, on honey bees; these compounds seems to cause neurotoxicity by increasing AChE activity [59,91], modulating CaE activity [55].…”

Section: Discussionmentioning

confidence: 99%

Review on Sublethal Effects of Environmental Contaminants in Honey Bees (Apis mellifera), Knowledge Gaps and Future Perspectives

Noi

Casini

Campani

et al. 2021

IJERPH

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Honey bees and the pollination services they provide are fundamental for agriculture and biodiversity. Agrochemical products and other classes of contaminants, such as trace elements and polycyclic aromatic hydrocarbons, contribute to the general decline of bees’ populations. For this reason, effects, and particularly sublethal effects of contaminants need to be investigated. We conducted a review of the existing literature regarding the type of effects evaluated in Apis mellifera, collecting information about regions, methodological approaches, the type of contaminants, and honey bees’ life stages. Europe and North America are the regions in which A. mellifera biological responses were mostly studied and the most investigated compounds are insecticides. A. mellifera was studied more in the laboratory than in field conditions. Through the observation of the different responses examined, we found that there were several knowledge gaps that should be addressed, particularly within enzymatic and molecular responses, such as those regarding the immune system and genotoxicity. The importance of developing an integrated approach that combines responses at different levels, from molecular to organism and population, needs to be highlighted in order to evaluate the impact of anthropogenic contamination on this pollinator species.

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Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees

Cited by 77 publications

References 93 publications

First application of an Integrated Biological Response index to assess the ecotoxicological status of honeybees from rural and urban areas

First application of an Integrated Biological Response index to assess the ecotoxicological status of honeybees from rural and urban areas

No evidence of effects or interaction between the widely used herbicide, glyphosate, and a common parasite in bumble bees

Review on Sublethal Effects of Environmental Contaminants in Honey Bees (Apis mellifera), Knowledge Gaps and Future Perspectives

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