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Dr. Luc P Belzunces
Laboratory of Environmental Toxicology, INRAE, UR 406 A&E, CS 40509, 84914 Avignon Cedex 9, France

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0 Neurotoxicology
0 Invertebrate toxicology
0 Effects and modes of action of pesticides
0 Mixtures of toxicants
0 Toxico-pathological interactions

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Effects and modes of action of pesticides

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Journal article
Published: 26 April 2021 in Ecotoxicology and Environmental Safety
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Pathogens and pollutants, such as pesticides, are potential stressors to all living organisms, including honey bees. Herbicides and fungicides are among the most prevalent pesticides in beehive matrices, and their interaction with Nosema ceranae is not well understood. In this study, the interactions between N. ceranae, the herbicide glyphosate and the fungicide difenoconazole were studied under combined sequential and overlapping exposure to the pesticides at a concentration of 0.1 µg/L in food. In the sequential exposure experiment, newly emerged bees were exposed to the herbicide from day 3 to day 13 after emerging and to the fungicide from day 13 to day 23. In the overlapping exposure experiment, bees were exposed to the herbicide from day 3 to day 13 and to the fungicide from day 7 to day 17. Infection by Nosema in early adult life stages (a few hours post emergence) greatly affected the survival of honey bees and elicited much higher mortality than was induced by pesticides either alone or in combination. Overlapping exposure to both pesticides induced higher mortality than was caused by sequential or individual exposure. Overlapping, but not sequential, exposure to pesticides synergistically increased the adverse effect of N. ceranae on honey bee longevity. The combination of Nosema and pesticides had a strong impact on physiological markers of the nervous system, detoxification, antioxidant defenses and social immunity of honey bees.

ACS Style

Hanine Almasri; Daiana Antonia Tavares; Marie Diogon; Maryline Pioz; Maryam Alamil; Déborah Sené; Sylvie Tchamitchian; Marianne Cousin; Jean-Luc Brunet; Luc P. Belzunces. Physiological effects of the interaction between Nosema ceranae and sequential and overlapping exposure to glyphosate and difenoconazole in the honey bee Apis mellifera. Ecotoxicology and Environmental Safety 2021, 217, 112258 .

AMA Style

Hanine Almasri, Daiana Antonia Tavares, Marie Diogon, Maryline Pioz, Maryam Alamil, Déborah Sené, Sylvie Tchamitchian, Marianne Cousin, Jean-Luc Brunet, Luc P. Belzunces. Physiological effects of the interaction between Nosema ceranae and sequential and overlapping exposure to glyphosate and difenoconazole in the honey bee Apis mellifera. Ecotoxicology and Environmental Safety. 2021; 217 ():112258.

Chicago/Turabian Style

Hanine Almasri; Daiana Antonia Tavares; Marie Diogon; Maryline Pioz; Maryam Alamil; Déborah Sené; Sylvie Tchamitchian; Marianne Cousin; Jean-Luc Brunet; Luc P. Belzunces. 2021. "Physiological effects of the interaction between Nosema ceranae and sequential and overlapping exposure to glyphosate and difenoconazole in the honey bee Apis mellifera." Ecotoxicology and Environmental Safety 217, no. : 112258.

Research article
Published: 06 April 2021 in Environmental Science and Pollution Research
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During all their life stages, bees are exposed to residual concentrations of pesticides, such as insecticides, herbicides, and fungicides, stored in beehive matrices. Fungicides are authorized for use during crop blooms because of their low acute toxicity to honey bees. Thus, a bee that might have been previously exposed to pesticides through contaminated food may be subjected to fungicide spraying when it initiates its first flight outside the hive. In this study, we assessed the effects of acute exposure to the fungicide in bees with different toxicological statuses. Three days after emergence, bees were subjected to chronic exposure to the insecticide imidacloprid and the herbicide glyphosate, either individually or in a binary mixture, at environmental concentrations of 0.01 and 0.1 μg/L in food (0.0083 and 0.083 μg/kg) for 30 days. Seven days after the beginning of chronic exposure to the pesticides (10 days after emergence), the bees were subjected to spraying with the fungicide difenoconazole at the registered field dosage. The results showed a delayed significant decrease in survival when honey bees were treated with the fungicide. Fungicide toxicity increased when honey bees were chronically exposed to glyphosate at the lowest concentration, decreased when they were exposed to imidacloprid, and did not significantly change when they were exposed to the binary mixture regardless of the concentration. Bees exposed to all of these pesticide combinations showed physiological disruptions, revealed by the modulation of several life history traits related mainly to metabolism, even when no effect of the other pesticides on fungicide toxicity was observed. These results show that the toxicity of active substances may be misestimated in the pesticide registration procedure, especially for fungicides.

ACS Style

Hanine Almasri; Daiana Antonia Tavares; Sylvie Tchamitchian; Michel Pélissier; Déborah Sené; Marianne Cousin; Jean-Luc Brunet; Luc P. Belzunces. Toxicological status changes the susceptibility of the honey bee Apis mellifera to a single fungicidal spray application. Environmental Science and Pollution Research 2021, 28, 42807 -42820.

AMA Style

Hanine Almasri, Daiana Antonia Tavares, Sylvie Tchamitchian, Michel Pélissier, Déborah Sené, Marianne Cousin, Jean-Luc Brunet, Luc P. Belzunces. Toxicological status changes the susceptibility of the honey bee Apis mellifera to a single fungicidal spray application. Environmental Science and Pollution Research. 2021; 28 (31):42807-42820.

Chicago/Turabian Style

Hanine Almasri; Daiana Antonia Tavares; Sylvie Tchamitchian; Michel Pélissier; Déborah Sené; Marianne Cousin; Jean-Luc Brunet; Luc P. Belzunces. 2021. "Toxicological status changes the susceptibility of the honey bee Apis mellifera to a single fungicidal spray application." Environmental Science and Pollution Research 28, no. 31: 42807-42820.

Review article
Published: 26 February 2021 in Chemosphere
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The growing gap between new evidence of pesticide toxicity in honeybees and conventional toxicological assays recommended by regulatory test guidelines emphasizes the need to complement current lethal endpoints with sublethal endpoints. In this context, behavioral and reproductive performances have received growing interest since the 2000s, likely due to their ecological relevance and/or the emergence of new technologies. We review the biological interests and methodological measurements of these predominantly studied endpoints and discuss their possible use in the pesticide risk assessment procedure based on their standardization level, simplicity and ecological relevance. It appears that homing flights and reproduction have great potential for pesticide risk assessment, mainly due to their ecological relevance. If exploratory research studies in ecotoxicology have paved the way toward a better understanding of pesticide toxicity in honeybees, the next objective will then be to translate the most relevant behavioral and reproductive endpoints into regulatory test methods. This will require more comparative studies and improving their ecological relevance. This latter goal may be facilitated by the use of population dynamics models for scaling up the consequences of adverse behavioral and reproductive effects from individuals to colonies.

ACS Style

Lena Barascou; Jean-Luc Brunet; Luc Belzunces; Axel Decourtye; Mickael Henry; Julie Fourrier; Yves Le Conte; Cedric Alaux. Pesticide risk assessment in honeybees: Toward the use of behavioral and reproductive performances as assessment endpoints. Chemosphere 2021, 276, 130134 .

AMA Style

Lena Barascou, Jean-Luc Brunet, Luc Belzunces, Axel Decourtye, Mickael Henry, Julie Fourrier, Yves Le Conte, Cedric Alaux. Pesticide risk assessment in honeybees: Toward the use of behavioral and reproductive performances as assessment endpoints. Chemosphere. 2021; 276 ():130134.

Chicago/Turabian Style

Lena Barascou; Jean-Luc Brunet; Luc Belzunces; Axel Decourtye; Mickael Henry; Julie Fourrier; Yves Le Conte; Cedric Alaux. 2021. "Pesticide risk assessment in honeybees: Toward the use of behavioral and reproductive performances as assessment endpoints." Chemosphere 276, no. : 130134.

Original article
Published: 03 February 2021 in Apidologie
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Pollinators foraging on monocultures like hybrid lavender are suspected to suffer physiological stress. We used biomarkers to assess changes in honeybee physiology pre- and post-hybrid lavender season, in high and low weight gain colonies. We observed post-season increased levels of enzymes involved in antioxidant defenses: catalase, superoxide dismutase, and glutathione peroxidase; increased levels of acetylcholinesterase, a biomarker of neural transmission; and decreased levels of alkaline phosphatase associated with the loss of midgut homeostasis. Compared to low weight gain colonies, high weight gain colonies showed lower levels of almost all analyzed biomarkers. We discuss the environmental and beekeeping factors likely underlying observed changes for which cause and effect remain to be established.

ACS Style

Claudia Dussaubat; Alban Maisonnasse; Luc P. Belzunces; Jean-Luc Brunet; André Kretzschtmar. Preliminary report of honeybee physiological changes pre- and post-hybrid lavender season in high and low weight gain colonies. Apidologie 2021, 52, 463 -472.

AMA Style

Claudia Dussaubat, Alban Maisonnasse, Luc P. Belzunces, Jean-Luc Brunet, André Kretzschtmar. Preliminary report of honeybee physiological changes pre- and post-hybrid lavender season in high and low weight gain colonies. Apidologie. 2021; 52 (2):463-472.

Chicago/Turabian Style

Claudia Dussaubat; Alban Maisonnasse; Luc P. Belzunces; Jean-Luc Brunet; André Kretzschtmar. 2021. "Preliminary report of honeybee physiological changes pre- and post-hybrid lavender season in high and low weight gain colonies." Apidologie 52, no. 2: 463-472.

Journal article
Published: 21 July 2020 in Ecotoxicology and Environmental Safety
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Multiple pesticides originating from plant protection treatments and the treatment of pests infecting honey bees are frequently detected in beehive matrices. Therefore, winter honey bees, which have a long life span, could be exposed to these pesticides for longer periods than summer honey bees. In this study, winter honey bees were exposed through food to the insecticide imidacloprid, the fungicide difenoconazole and the herbicide glyphosate, alone or in binary and ternary mixtures, at environmental concentrations (0 (controls), 0.1, 1 and 10 μg/L) for 20 days. The survival of the honey bees was significantly reduced after exposure to these 3 pesticides individually and in combination. Overall, the combinations had a higher impact than the pesticides alone with a maximum mortality of 52.9% after 20 days of exposure to the insecticide-fungicide binary mixture at 1 μg/L. The analyses of the surviving bees showed that these different pesticide combinations had a systemic global impact on the physiological state of the honey bees, as revealed by the modulation of head, midgut and abdomen glutathione-S-transferase, head acetylcholinesterase, abdomen glucose-6-phosphate dehydrogenase and midgut alkaline phosphatase, which are involved in the detoxification of xenobiotics, the nervous system, defenses against oxidative stress, metabolism and immunity, respectively. These results demonstrate the importance of studying the effects of chemical cocktails based on low realistic exposure levels and developing long-term tests to reveal possible lethal and adverse sublethal interactions in honey bees and other insect pollinators.

ACS Style

Hanine Almasri; Daiana Antonia Tavares; Maryline Pioz; Déborah Sené; Sylvie Tchamitchian; Marianne Cousin; Jean-Luc Brunet; Luc P. Belzunces. Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees. Ecotoxicology and Environmental Safety 2020, 203, 111013 .

AMA Style

Hanine Almasri, Daiana Antonia Tavares, Maryline Pioz, Déborah Sené, Sylvie Tchamitchian, Marianne Cousin, Jean-Luc Brunet, Luc P. Belzunces. Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees. Ecotoxicology and Environmental Safety. 2020; 203 ():111013.

Chicago/Turabian Style

Hanine Almasri; Daiana Antonia Tavares; Maryline Pioz; Déborah Sené; Sylvie Tchamitchian; Marianne Cousin; Jean-Luc Brunet; Luc P. Belzunces. 2020. "Mixtures of an insecticide, a fungicide and a herbicide induce high toxicities and systemic physiological disturbances in winter Apis mellifera honey bees." Ecotoxicology and Environmental Safety 203, no. : 111013.

Original research article
Published: 27 August 2019 in Journal of Apicultural Research
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Neonicotinoids can cause a variety of adverse sublethal effects in workers and queens honey bees. However, despite their key role in reproduction, drones have not received much attention on how neonicotinoids can affect their fertility. The aim of this study was to assess the influence of clothianidin exposure of drones at sexual maturity stage, on antioxidant enzyme activities, malondialdehyde (MDA) level and on protein content of semen. Our results show for the first time that clothianidin elicits significant increases in superoxide dismutase, of glutathione peroxidase, of catalase and of MDA level. Protein content in semen of drones exposed to clothianidin was significantly decreased. This study suggested that drones exposed to clothianidin at the stage of sexual maturity could induce oxidative stress in spermatozoa of drones which could affect the semen quality and therefore the queen fecundity.

ACS Style

Faten Ben Abdelkader; Guillaume Kairo; Marc Bonnet; Naima Barbouche; Luc P Belzunces; Jean Luc Brunet. Effects of clothianidin on antioxidant enzyme activities and malondialdehyde level in honey bee drone semen. Journal of Apicultural Research 2019, 58, 740 -745.

AMA Style

Faten Ben Abdelkader, Guillaume Kairo, Marc Bonnet, Naima Barbouche, Luc P Belzunces, Jean Luc Brunet. Effects of clothianidin on antioxidant enzyme activities and malondialdehyde level in honey bee drone semen. Journal of Apicultural Research. 2019; 58 (5):740-745.

Chicago/Turabian Style

Faten Ben Abdelkader; Guillaume Kairo; Marc Bonnet; Naima Barbouche; Luc P Belzunces; Jean Luc Brunet. 2019. "Effects of clothianidin on antioxidant enzyme activities and malondialdehyde level in honey bee drone semen." Journal of Apicultural Research 58, no. 5: 740-745.

Journal article
Published: 27 February 2019 in Ecotoxicology and Environmental Safety
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Terrestrial ecosystems are exposed to various kinds of pollutants, including radionuclides. The honeybee, Apis mellifera, is commonly used in ecotoxicology as a model species for evaluating the effects of pollutants. In the present study, honeybees were irradiated right after birth for 14 days with gamma rays at dose rates ranging between 4.38 × 10−3 and 588 mGy/d. Biological tissues (head, intestine and abdomen) were sampled at D3, D10 and D14. Ten different physiological markers involved in nervous (acetylcholinesterase (AChE)), antioxidative (catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GPx) and glutathione-S-transferase (GST)), immune system (phenoloxidase (PO)) and metabolism (carboxylesterases (CaEs) and alkaline phosphatase (ALP)) were measured. Univariate analyses were conducted to determine whether each individual biomarker response was positively or negatively correlated with the dose rate. Then, multivariate analyses were applied to investigate the relationships between all the biomarker responses. Although no mortality occurred during the experiment, several biomarkers varied significantly in relation to the dose rate. Globally, the biomarkers of antioxidant and immune systems decreased as the dose rate increased. Reversible effects on the indicator of the neural system were found. Concerning indicators of metabolism (carboxylesterases), variations occurred but no clear pattern was found. Taken altogether, these results help better understand the effects of ionizing radiation on bees by identifying relevant physiological markers of effects. These results could improve the assessment of the environmental risk due to ionizing radiation in terrestrial ecosystems.

ACS Style

B. Gagnaire; M. Bonnet; S. Tchamitchian; I. Cavalié; C. Della-Vedova; N. Dubourg; C. Adam-Guillermin; J.-L. Brunet; L.P. Belzunces. Physiological effects of gamma irradiation in the honeybee, Apis mellifera. Ecotoxicology and Environmental Safety 2019, 174, 153 -163.

AMA Style

B. Gagnaire, M. Bonnet, S. Tchamitchian, I. Cavalié, C. Della-Vedova, N. Dubourg, C. Adam-Guillermin, J.-L. Brunet, L.P. Belzunces. Physiological effects of gamma irradiation in the honeybee, Apis mellifera. Ecotoxicology and Environmental Safety. 2019; 174 ():153-163.

Chicago/Turabian Style

B. Gagnaire; M. Bonnet; S. Tchamitchian; I. Cavalié; C. Della-Vedova; N. Dubourg; C. Adam-Guillermin; J.-L. Brunet; L.P. Belzunces. 2019. "Physiological effects of gamma irradiation in the honeybee, Apis mellifera." Ecotoxicology and Environmental Safety 174, no. : 153-163.

Research article
Published: 22 July 2018 in Pest Management Science
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BACKGROUND Vector‐borne diseases are of high concern for human, animal and plant health. In humans, such diseases are often transmitted by flying insects. Flying insects stop their flight when their kinetic energy cannot compensate for the wind speed. Here, the efficiency of an air curtain in preventing insects from entering a building was studied using the honey bee as a model. RESULTS Bees were trained to visit a food source placed in a building. The air curtain was tested with strongly motivated bees, when the visiting activity was very high. Airflow velocity was modulated by setting an air curtain device at different voltages. At the nominal voltage, the anti‐insect efficiency was 99.9 ± 0.2% compared with both the number of bees at a given time in the absence of the air curtain and the number of bees before the activation of the air curtain. The efficiency decreased as the airflow velocity decreased. CONCLUSION The results show that an air curtain operating at an airflow velocity of 7.5 m/sec may prevent a strong flyer with high kinetic energy, such as the honey bee, from entering a building. Thus, air curtains offer an alternative approach for combating vector‐borne diseases. This article is protected by copyright. All rights reserved.

ACS Style

Guillaume Kairo; Maryline Pioz; Sylvie Tchamitchian; Michel Pelissier; Jean-Luc Brunet; Luc P. Belzunces. Efficiency of an air curtain as an anti-insect barrier: the honey bee as a model insect. Pest Management Science 2018, 74, 2707 -2715.

AMA Style

Guillaume Kairo, Maryline Pioz, Sylvie Tchamitchian, Michel Pelissier, Jean-Luc Brunet, Luc P. Belzunces. Efficiency of an air curtain as an anti-insect barrier: the honey bee as a model insect. Pest Management Science. 2018; 74 (12):2707-2715.

Chicago/Turabian Style

Guillaume Kairo; Maryline Pioz; Sylvie Tchamitchian; Michel Pelissier; Jean-Luc Brunet; Luc P. Belzunces. 2018. "Efficiency of an air curtain as an anti-insect barrier: the honey bee as a model insect." Pest Management Science 74, no. 12: 2707-2715.

Journal article
Published: 01 October 2017 in Environmental Pollution
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Under laboratory conditions, the effects of thiamethoxam were investigated in larvae, pupae and emerging honey bees after exposure at larval stages with different concentrations in the food (0.00001 ng/μL, 0.001 ng/μL and 1.44 ng/μL). Thiamethoxam reduced the survival of larvae and pupae and consequently decreased the percentage of emerging honey bees. Thiamethoxam induced important physiological disturbances. It increased acetylcholinesterase (AChE) activity at all developmental stages and increased glutathione-S-transferase (GST) and carboxylesterase para (CaEp) activities at the pupal stages. For midgut alkaline phosphatase (ALP), no activity was detected in pupae stages, and no effect was observed in larvae and emerging bees. We assume that the effects of thiamethoxam on the survival, emergence and physiology of honey bees may affect the development of the colony. These results showed that attention should be paid to the exposure to pesticides during the developmental stages of the honey bee. This study represents the first investigation of the effects of thiamethoxam on the development of A. mellifera following larval exposure.

ACS Style

Daiana Antonia Tavares; Claudia Dussaubat; André Kretzschmar; Stephan Malfitano Carvalho; Elaine C.M. Silva-Zacarin; Osmar Malaspina; Géraldine Bérail; Jean-Luc Brunet; Luc P. Belzunces. Exposure of larvae to thiamethoxam affects the survival and physiology of the honey bee at post-embryonic stages. Environmental Pollution 2017, 229, 386 -393.

AMA Style

Daiana Antonia Tavares, Claudia Dussaubat, André Kretzschmar, Stephan Malfitano Carvalho, Elaine C.M. Silva-Zacarin, Osmar Malaspina, Géraldine Bérail, Jean-Luc Brunet, Luc P. Belzunces. Exposure of larvae to thiamethoxam affects the survival and physiology of the honey bee at post-embryonic stages. Environmental Pollution. 2017; 229 ():386-393.

Chicago/Turabian Style

Daiana Antonia Tavares; Claudia Dussaubat; André Kretzschmar; Stephan Malfitano Carvalho; Elaine C.M. Silva-Zacarin; Osmar Malaspina; Géraldine Bérail; Jean-Luc Brunet; Luc P. Belzunces. 2017. "Exposure of larvae to thiamethoxam affects the survival and physiology of the honey bee at post-embryonic stages." Environmental Pollution 229, no. : 386-393.

Journal article
Published: 01 August 2016 in Chemosphere
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Boscalid is a new-generation fungicide that has been detected in several bee matrices. The objective of this work was to characterize boscalid metabolites in honeybees based on in vivo experimentation, and next to verify the presence of theses metabolites into honeybees from colonies presenting troubles. A methodology based on complementary mass spectrometric tools, namely ultra-high performance liquid chromatography coupled to high-resolution mass spectrometry (UHPLC-QToF) or triple quadrupole mass spectrometry (UHPLC-QqQ) was implemented. Honeybees were sprayed with boscalid, at field rate (to induce the metabolization process) and the parent compound with its generated metabolites were then extracted using modified EU-QuEChERS method. The mass characteristics including exact mass, isotopic profile and mass fragments allowed assuming the structure of several metabolites. Some of them were unambiguously identified by comparison with synthesized analytical standards. The metabolites were resulted from hydroxylation and dechlorination of the parent compound as well as the substitution of a chlorine atom with an hydroxyl group. The metabolites were then quantified in bee samples collected from various beehives located in France. Boscalid and three of its metabolites were present in some samples at a level ranged between 0.2 and 36.3 ng/g.

ACS Style

Claire Jabot; Gaëlle Daniele; Barbara Giroud; Sylvie Tchamitchian; Luc P. Belzunces; Hervé Casabianca; Emmanuelle Vulliet. Detection and quantification of boscalid and its metabolites in honeybees. Chemosphere 2016, 156, 245 -251.

AMA Style

Claire Jabot, Gaëlle Daniele, Barbara Giroud, Sylvie Tchamitchian, Luc P. Belzunces, Hervé Casabianca, Emmanuelle Vulliet. Detection and quantification of boscalid and its metabolites in honeybees. Chemosphere. 2016; 156 ():245-251.

Chicago/Turabian Style

Claire Jabot; Gaëlle Daniele; Barbara Giroud; Sylvie Tchamitchian; Luc P. Belzunces; Hervé Casabianca; Emmanuelle Vulliet. 2016. "Detection and quantification of boscalid and its metabolites in honeybees." Chemosphere 156, no. : 245-251.

Journal article
Published: 01 May 2016 in Ecotoxicology and Environmental Safety
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In the agricultural environment, honey bees may be exposed to combinations of pesticides. Until now, the effects of these combinations on honey bee health have been poorly investigated. In this study, we assessed the impacts of biological and chemical insecticides, combining low dietary concentrations of Bacillus thuringiensis (Bt) spores (100 and 1000 µg/L) with the chemical insecticide fipronil (1 µg/L). In order to assess the possible effects of Cry toxins, the Bt kurstaki strain (Btk) was compared with a Bt strain devoid of toxin-encoding plasmids (Bt Cry−). The oral exposure to fipronil and Bt spores from both strains for 10 days did not elicit significant effects on the feeding behavior and survival after 25 days. Local and systemic physiological effects were investigated by measuring the activities of enzymes involved in the intermediary and detoxication metabolisms at two sampling dates (day 10 and day 20). Attention was focused on head and midgut glutathione-S-transferase (GST), midgut alkaline phosphatase (ALP), abdomen glyceraldehyde-3-phosphate dehydrogenase (GAPD) and glucose-6-phosphate dehydrogenase (G6PD). We found that Bt Cry− and Btk spores induced physiological modifications by differentially modulating enzyme activities. Fipronil influenced the enzyme activities differently at days 10 and 20 and, when combined with Bt spores, elicited modulations of some spore-induced physiological responses. These results show that an apparent absence of toxicity may hide physiological disruptions that could be potentially damaging for the bees, especially in the case of combined exposures to other environmental stressors.

ACS Style

Maria Teresa Renzi; Marcel Amichot; David Pauron; Sylvie Tchamitchian; Jean-Luc Brunet; André Kretzschmar; Stefano Maini; Luc P. Belzunces. Chronic toxicity and physiological changes induced in the honey bee by the exposure to fipronil and Bacillus thuringiensis spores alone or combined. Ecotoxicology and Environmental Safety 2016, 127, 205 -213.

AMA Style

Maria Teresa Renzi, Marcel Amichot, David Pauron, Sylvie Tchamitchian, Jean-Luc Brunet, André Kretzschmar, Stefano Maini, Luc P. Belzunces. Chronic toxicity and physiological changes induced in the honey bee by the exposure to fipronil and Bacillus thuringiensis spores alone or combined. Ecotoxicology and Environmental Safety. 2016; 127 ():205-213.

Chicago/Turabian Style

Maria Teresa Renzi; Marcel Amichot; David Pauron; Sylvie Tchamitchian; Jean-Luc Brunet; André Kretzschmar; Stefano Maini; Luc P. Belzunces. 2016. "Chronic toxicity and physiological changes induced in the honey bee by the exposure to fipronil and Bacillus thuringiensis spores alone or combined." Ecotoxicology and Environmental Safety 127, no. : 205-213.

Journal article
Published: 30 June 2015 in Environmental Toxicology and Chemistry
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In pesticide risk assessment, the estimation of the routes and levels of exposure is critical. For honey bees, the toxicity of pesticides is assessed by thorax contact to account for all possible contact exposures of bees subjected to a pesticide spray. In this study, we tested 6 different active substances with different hydrophobicity, and for the first time, we demonstrated that it is possible to induce mortality by pesticide contact with only the wings of the honey bee. The toxicities induced by contact with the wings and thorax were similar, with the wing median lethal dose (LD50) being 0.99‐2.23 times higher than that of the thorax, which demonstrates that the wings represent a relevant route of exposure in the honey bee. In a second approach, we estimated the air volume displaced by the wings during one beating cycle to be 0.51 ± 0.03 cm3, which corresponds to a volume of 116.8 ± 5.8 cm3 s‐1 at a wing beat frequency of 230 Hz. Then, we tested realistic scenarios of exposure for a bee flying through a pesticide cloud at different concentrations. In the worst‐case scenario, the dose accumulated during the flight reached 525 ng bee‐1 s‐1. These results show that the procedure used to assess the risk posed by contact with pesticides could be improved by accounting for wing exposure. This article is protected by copyright. All rights reserved

ACS Style

Yannick Poquet; Guillaume Kairo; Sylvie Tchamitchian; Jean-Luc Brunet; Luc P. Belzunces. Wings as a new route of exposure to pesticides in the honey bee. Environmental Toxicology and Chemistry 2015, 34, 1983 -1988.

AMA Style

Yannick Poquet, Guillaume Kairo, Sylvie Tchamitchian, Jean-Luc Brunet, Luc P. Belzunces. Wings as a new route of exposure to pesticides in the honey bee. Environmental Toxicology and Chemistry. 2015; 34 (9):1983-1988.

Chicago/Turabian Style

Yannick Poquet; Guillaume Kairo; Sylvie Tchamitchian; Jean-Luc Brunet; Luc P. Belzunces. 2015. "Wings as a new route of exposure to pesticides in the honey bee." Environmental Toxicology and Chemistry 34, no. 9: 1983-1988.

Journal article
Published: 23 February 2015 in The Open Entomology Journal
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Larvicidal Activity of a Natural Botanical Biostop Moustiques® and Physiological Changes Induced in Susceptible and Resistant Strains of Anopheles gambiae Giles (Diptera: Culicidae)

ACS Style

Guillaume K. Ketoh; Koffi M. Ahadji-Dabla; Jean-Luc Brunet; Georges Y. Apétogbo; Isabelle A. Glitho; Luc P. Belzunces. Larvicidal Activity of a Natural Botanical Biostop Moustiques®and Physiological Changes Induced in Susceptible and Resistant Strains of Anopheles gambiae Giles (Diptera: Culicidae). The Open Entomology Journal 2015, 9, 12 -19.

AMA Style

Guillaume K. Ketoh, Koffi M. Ahadji-Dabla, Jean-Luc Brunet, Georges Y. Apétogbo, Isabelle A. Glitho, Luc P. Belzunces. Larvicidal Activity of a Natural Botanical Biostop Moustiques®and Physiological Changes Induced in Susceptible and Resistant Strains of Anopheles gambiae Giles (Diptera: Culicidae). The Open Entomology Journal. 2015; 9 (1):12-19.

Chicago/Turabian Style

Guillaume K. Ketoh; Koffi M. Ahadji-Dabla; Jean-Luc Brunet; Georges Y. Apétogbo; Isabelle A. Glitho; Luc P. Belzunces. 2015. "Larvicidal Activity of a Natural Botanical Biostop Moustiques®and Physiological Changes Induced in Susceptible and Resistant Strains of Anopheles gambiae Giles (Diptera: Culicidae)." The Open Entomology Journal 9, no. 1: 12-19.

Review
Published: 11 February 2015 in Environmental Health
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Experimental studies investigating the effects of endocrine disruptors frequently identify potential unconventional dose-response relationships called non-monotonic dose-response (NMDR) relationships. Standardized approaches for investigating NMDR relationships in a risk assessment context are missing. The aim of this work was to develop criteria for assessing the strength of NMDR relationships. A literature search was conducted to identify published studies that report NMDR relationships with endocrine disruptors. Fifty-one experimental studies that investigated various effects associated with endocrine disruption elicited by many substances were selected. Scoring criteria were applied by adaptation of an approach previously used for identification of hormesis-type dose-response relationships. Out of the 148 NMDR relationships analyzed, 82 were categorized with this method as having a "moderate" to "high" level of plausibility for various effects. Numerous modes of action described in the literature can explain such phenomena. NMDR can arise from numerous molecular mechanisms such as opposing effects induced by multiple receptors differing by their affinity, receptor desensitization, negative feedback with increasing dose, or dose-dependent metabolism modulation. A stepwise decision tree was developed as a tool to standardize the analysis of NMDR relationships observed in the literature with the final aim to use these results in a Risk Assessment purpose. This decision tree was finally applied to studies focused on the effects of bisphenol A.

ACS Style

Fabien Lagarde; Claire Beausoleil; Scott Belcher; Luc P Belzunces; Claude Emond; Michel Guerbet; Christophe Rousselle. Non-monotonic dose-response relationships and endocrine disruptors: a qualitative method of assessment. Environmental Health 2015, 14, 13 -13.

AMA Style

Fabien Lagarde, Claire Beausoleil, Scott Belcher, Luc P Belzunces, Claude Emond, Michel Guerbet, Christophe Rousselle. Non-monotonic dose-response relationships and endocrine disruptors: a qualitative method of assessment. Environmental Health. 2015; 14 (1):13-13.

Chicago/Turabian Style

Fabien Lagarde; Claire Beausoleil; Scott Belcher; Luc P Belzunces; Claude Emond; Michel Guerbet; Christophe Rousselle. 2015. "Non-monotonic dose-response relationships and endocrine disruptors: a qualitative method of assessment." Environmental Health 14, no. 1: 13-13.

Research article
Published: 20 November 2014 in PLOS ONE
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Plant protection spray treatments may expose non-target organisms to pesticides. In the pesticide registration procedure, the honey bee represents one of the non-target model species for which the risk posed by pesticides must be assessed on the basis of the hazard quotient (HQ). The HQ is defined as the ratio between environmental exposure and toxicity. For the honey bee, the HQ calculation is not consistent because it corresponds to the ratio between the pesticide field rate (in mass of pesticide/ha) and LD50 (in mass of pesticide/bee). Thus, in contrast to all other species, the HQ can only be interpreted empirically because it corresponds to a number of bees/ha. This type of HQ calculation is due to the difficulty in transforming pesticide field rates into doses to which bees are exposed. In this study, we used a pragmatic approach to determine the apparent exposure surface area of honey bees submitted to pesticide treatments by spraying with a Potter-type tower. The doses received by the bees were quantified by very efficient chemical analyses, which enabled us to determine an apparent surface area of 1.05 cm2/bee. The apparent surface area was used to calculate the exposure levels of bees submitted to pesticide sprays and then to revisit the HQ ratios with a calculation mode similar to that used for all other living species. X-tomography was used to assess the physical surface area of a bee, which was 3.27 cm2/bee, and showed that the apparent exposure surface was not overestimated. The control experiments showed that the toxicity induced by doses calculated with the exposure surface area was similar to that induced by treatments according to the European testing procedure. This new approach to measure risk is more accurate and could become a tool to aid the decision-making process in the risk assessment of pesticides.

ACS Style

Yannick Poquet; Laurent Bodin; Marc Tchamitchian; Marion Fusellier; Barbara Giroud; Florent Lafay; Audrey Bulete; Sylvie Tchamitchian; Marianne Cousin; Michel Pelissier; Jean-Luc Brunet; Luc P. Belzunces. A Pragmatic Approach to Assess the Exposure of the Honey Bee (Apis mellifera) When Subjected to Pesticide Spray. PLOS ONE 2014, 9, e113728 .

AMA Style

Yannick Poquet, Laurent Bodin, Marc Tchamitchian, Marion Fusellier, Barbara Giroud, Florent Lafay, Audrey Bulete, Sylvie Tchamitchian, Marianne Cousin, Michel Pelissier, Jean-Luc Brunet, Luc P. Belzunces. A Pragmatic Approach to Assess the Exposure of the Honey Bee (Apis mellifera) When Subjected to Pesticide Spray. PLOS ONE. 2014; 9 (11):e113728.

Chicago/Turabian Style

Yannick Poquet; Laurent Bodin; Marc Tchamitchian; Marion Fusellier; Barbara Giroud; Florent Lafay; Audrey Bulete; Sylvie Tchamitchian; Marianne Cousin; Michel Pelissier; Jean-Luc Brunet; Luc P. Belzunces. 2014. "A Pragmatic Approach to Assess the Exposure of the Honey Bee (Apis mellifera) When Subjected to Pesticide Spray." PLOS ONE 9, no. 11: e113728.

Journal article
Published: 21 November 2013 in Analytical and Bioanalytical Chemistry
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Several methods for analyzing pesticides in honey have been developed. However, they do not always reach the sufficiently low limits of quantification (LOQ) needed to quantify pesticides toxic to honey bees at low doses. To properly evaluate the toxicity of pesticides, LOQ have to reach at least 1 ng/g. In this context, we developed extraction and analytical methods for the simultaneous detection of 22 relevant insecticides belonging to three chemical families (neonicotinoids, pyrethroids, and pyrazoles) in honey. The insecticides were extracted with the QuEChERS method that consists in an extraction and a purification with mixtures of salts adapted to the matrix and the substances to be extracted. Analyses were performed by gas chromatography coupled with tandem mass spectrometry (GC-MS/MS) for the pyrazoles and the pyrethroids and by high-performance liquid chromatography coupled with tandem mass spectrometry (HPLC-MS/MS) for the neonicotinoids and ethiprole. Calibration curves were built from various honey types fortified at different concentrations. Linear responses were obtained between 0.2 and 5 ng/g. Limits of detection (LOD) ranged between 0.07 and 0.2 ng/g, and LOQ ranged between 0.2 and 0.5 ng/g. The mean extraction yields ranged between 63 % and 139 % with RSD Figure

ACS Style

Delphine Paradis; Géraldine Bérail; Jean-Marc Bonmatin; Luc P. Belzunces. Sensitive analytical methods for 22 relevant insecticides of 3 chemical families in honey by GC-MS/MS and LC-MS/MS. Analytical and Bioanalytical Chemistry 2013, 406, 621 -633.

AMA Style

Delphine Paradis, Géraldine Bérail, Jean-Marc Bonmatin, Luc P. Belzunces. Sensitive analytical methods for 22 relevant insecticides of 3 chemical families in honey by GC-MS/MS and LC-MS/MS. Analytical and Bioanalytical Chemistry. 2013; 406 (2):621-633.

Chicago/Turabian Style

Delphine Paradis; Géraldine Bérail; Jean-Marc Bonmatin; Luc P. Belzunces. 2013. "Sensitive analytical methods for 22 relevant insecticides of 3 chemical families in honey by GC-MS/MS and LC-MS/MS." Analytical and Bioanalytical Chemistry 406, no. 2: 621-633.

Journal article
Published: 30 August 2013 in Environment International
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The aim of this study was to distinguish the impacts of two different anthropogenic conditions using the honeybee Apis mellifera as a bioindicator associated with a battery of biomarkers previously validated in the laboratory. Both the urban (RAV, Ravine des Cabris) and semi-natural (CIL, Cilaos) sites in La Reunion Island were compared in order to assess the impacts of two types of local pollution using the discriminating potential of biomarkers. Hives were placed at the CIL and RAV sites and honeybees were collected from each hive every three months over one year. Honeybee responses were evaluated with respect to several biochemical biomarkers: glutathione-S-transferase (GST), acetylcholinesterase (AChE), alkaline phosphatase (ALP) and metallothioneins (MT). The results showed a significant difference between the localities in terms of GST, AChE and ALP activities, as regarding midgut MT tissue levels. Compared to the CIL site, ALP and MT tissue levels were higher at the RAV site, although AChE activity was lower. GST displayed more contrasted effects. These results strongly suggest that the honeybees based in the more anthropized area were subjected to sublethal stress involving both oxidative stress and detoxification processes with the occurrence of neurotoxic pollutants, amongst which metals were good candidates. A classification tree enabled defining a decision procedure to distinguish the sampling locations and enabled excellent classification accuracy (89%) for the data set. This field study constitutes a strong support in favour of the in situ assessment of environmental quality using honeybee biomarkers and validates the possibility of performing further ecotoxicological studies using honeybee biomarkers.

ACS Style

A. Badiou-Bénéteau; A. Benneveau; F. Géret; H. Delatte; N. Becker; J.L. Brunet; B. Reynaud; L.P. Belzunces. Honeybee biomarkers as promising tools to monitor environmental quality. Environment International 2013, 60, 31 -41.

AMA Style

A. Badiou-Bénéteau, A. Benneveau, F. Géret, H. Delatte, N. Becker, J.L. Brunet, B. Reynaud, L.P. Belzunces. Honeybee biomarkers as promising tools to monitor environmental quality. Environment International. 2013; 60 ():31-41.

Chicago/Turabian Style

A. Badiou-Bénéteau; A. Benneveau; F. Géret; H. Delatte; N. Becker; J.L. Brunet; B. Reynaud; L.P. Belzunces. 2013. "Honeybee biomarkers as promising tools to monitor environmental quality." Environment International 60, no. : 31-41.

Research article
Published: 28 May 2013 in PLOS ONE
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The effects of the herbicide Paraquat were investigated in honey bee larvae with attention focused on oenocytes. Honey bee larvae were exposed to Paraquat at different concentrations in the food: 0, 0.001, 0.01, 0.1 and 1 µg/kg. In controls, between 24 h and 48 h, oenocytes grew from 630.1 to 1643.8 µm2 while nuclei changed in size from 124.9 to 245.6 µm2. At 24 h, Paraquat induced a slight decrease in the size of oenocytes and nuclei. N-acetylcysteine (NAC), an antioxidant substance, slightly lowered the effects of Paraquat. At 48 h, Paraquat elicited a strong concentration-dependent decrease in the size of oenocytes, even at the lowest concentration. NAC reversed the effect of Paraquat at a concentration of ≥0.01 µg/kg. This reversion suggested different modes of action of Paraquat, with an oxidant action prevalent at concentrations ≥0.01 µg/kg. This study is the first which reports an effect of a pesticide at the very low concentration of 1 ng/kg, a concentration below the detection limits of the most efficient analytic methods. It shows that chemicals, including pesticides, are likely to have a potential impact at such exposure levels. We also suggest that Paraquat could be used as a suitable tool for investigating the functions of oenocytes.

ACS Style

Marianne Cousin; Elaine Silva-Zacarin; André Kretzschmar; Mohamed El Maataoui; Jean-Luc Brunet; Luc P. Belzunces. Size Changes in Honey Bee Larvae Oenocytes Induced by Exposure to Paraquat at Very Low Concentrations. PLOS ONE 2013, 8, e65693 .

AMA Style

Marianne Cousin, Elaine Silva-Zacarin, André Kretzschmar, Mohamed El Maataoui, Jean-Luc Brunet, Luc P. Belzunces. Size Changes in Honey Bee Larvae Oenocytes Induced by Exposure to Paraquat at Very Low Concentrations. PLOS ONE. 2013; 8 (5):e65693.

Chicago/Turabian Style

Marianne Cousin; Elaine Silva-Zacarin; André Kretzschmar; Mohamed El Maataoui; Jean-Luc Brunet; Luc P. Belzunces. 2013. "Size Changes in Honey Bee Larvae Oenocytes Induced by Exposure to Paraquat at Very Low Concentrations." PLOS ONE 8, no. 5: e65693.

Environmental toxicology
Published: 24 May 2013 in Environmental Toxicology and Chemistry
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The present study was intended to evaluate the responses of enzymes in the honeybee Apis mellifera after exposure to deltamethrin, fipronil, and spinosad and their use as biomarkers. After determination of the median lethal doses (LD50), honeybees were exposed at doses of 5.07 ng/bee and 2.53 ng/bee for deltamethrin, 0.58 ng/bee and 0.29 ng/bee for fipronil, and 4.71 ng/bee and 2.36 ng/bee for spinosad (equivalent to 1/10th [LD50/10] and 1/20th [LD50/20] of the LD50, respectively). The responses of acetylcholinesterase (AChE), carboxylesterases (CaEs‐1–3), glutathione‐S‐transferase (GST), catalase (CAT), and alkaline phosphatase (ALP) were assessed. The results showed that deltamethrin, fipronil, and spinosad modulated these biomarkers differentially. For the enzyme involved in the defense against oxidative stress, fipronil and spinosad induced CAT activity. For the remaining enzymes, 3 response profiles were identified. First, exposure to deltamethrin induced slight effects and modulated only CaE‐1 and CaE‐2, with opposite effects. Second, spinosad exhibited an induction profile for most of the biomarkers, except AChE. Third, fipronil did not modulate AChE, CaE‐2, or GST, increased CAT and CaE‐1, and decreased ALP. Thus, this set of honeybee biomarkers appears to be a promising tool to evaluate environmental and honeybee health, and it could generate fingerprints to characterize exposures to pesticides. Environ Toxicol Chem 2013;32:2117–2124. © 2013 SETAC

ACS Style

Stephan M. Carvalho; Luc P. Belzunces; Geraldo A. Carvalho; Jean-Luc Brunet; Alexandra Badiou-Beneteau. Enzymatic biomarkers as tools to assess environmental quality: A case study of exposure of the honeybeeApis melliferato insecticides. Environmental Toxicology and Chemistry 2013, 32, 2117 -2124.

AMA Style

Stephan M. Carvalho, Luc P. Belzunces, Geraldo A. Carvalho, Jean-Luc Brunet, Alexandra Badiou-Beneteau. Enzymatic biomarkers as tools to assess environmental quality: A case study of exposure of the honeybeeApis melliferato insecticides. Environmental Toxicology and Chemistry. 2013; 32 (9):2117-2124.

Chicago/Turabian Style

Stephan M. Carvalho; Luc P. Belzunces; Geraldo A. Carvalho; Jean-Luc Brunet; Alexandra Badiou-Beneteau. 2013. "Enzymatic biomarkers as tools to assess environmental quality: A case study of exposure of the honeybeeApis melliferato insecticides." Environmental Toxicology and Chemistry 32, no. 9: 2117-2124.

Journal article
Published: 01 January 2013 in Journal of Apicultural Research
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IBRA, the world's longest established apicultural research publishers, promotes the value of bees by providing information on bee science and beekeeping worldwide. A not-for-profit organisation founded in 1949

ACS Style

Piotr Medrzycki; Hervé Giffard; Pierrick Aupinel; Luc P Belzunces; Marie-Pierre Chauzat; Christian Claßen; Marc E Colin; Thierry Dupont; Vincenzo Girolami; Reed Johnson; Yves Le Conte; Johannes Lückmann; Matteo Marzaro; Jens Pistorius; Claudio Porrini; Andrea Schur; Fabio Sgolastra; Noa Simon Delso; Jozef J M Van Der Steen; Klaus Wallner; Cedric Alaux; David G Biron; Nicolas Blot; Gherardo Bogo; Jean-Luc Brunet; Frédéric Delbac; Marie Diogon; Hicham El Alaoui; Bertille Provost; Simone Tosi; Cyril Vidau. Standard methods for toxicology research inApis mellifera. Journal of Apicultural Research 2013, 52, 1 -60.

AMA Style

Piotr Medrzycki, Hervé Giffard, Pierrick Aupinel, Luc P Belzunces, Marie-Pierre Chauzat, Christian Claßen, Marc E Colin, Thierry Dupont, Vincenzo Girolami, Reed Johnson, Yves Le Conte, Johannes Lückmann, Matteo Marzaro, Jens Pistorius, Claudio Porrini, Andrea Schur, Fabio Sgolastra, Noa Simon Delso, Jozef J M Van Der Steen, Klaus Wallner, Cedric Alaux, David G Biron, Nicolas Blot, Gherardo Bogo, Jean-Luc Brunet, Frédéric Delbac, Marie Diogon, Hicham El Alaoui, Bertille Provost, Simone Tosi, Cyril Vidau. Standard methods for toxicology research inApis mellifera. Journal of Apicultural Research. 2013; 52 (4):1-60.

Chicago/Turabian Style

Piotr Medrzycki; Hervé Giffard; Pierrick Aupinel; Luc P Belzunces; Marie-Pierre Chauzat; Christian Claßen; Marc E Colin; Thierry Dupont; Vincenzo Girolami; Reed Johnson; Yves Le Conte; Johannes Lückmann; Matteo Marzaro; Jens Pistorius; Claudio Porrini; Andrea Schur; Fabio Sgolastra; Noa Simon Delso; Jozef J M Van Der Steen; Klaus Wallner; Cedric Alaux; David G Biron; Nicolas Blot; Gherardo Bogo; Jean-Luc Brunet; Frédéric Delbac; Marie Diogon; Hicham El Alaoui; Bertille Provost; Simone Tosi; Cyril Vidau. 2013. "Standard methods for toxicology research inApis mellifera." Journal of Apicultural Research 52, no. 4: 1-60.