The Herbicide Glyphosate Negatively Affects Midgut Bacterial Communities and Survival of Honey Bee during Larvae Reared in Vitro
- Pingli Dai*Pingli Dai*E-mail: [email protected]. Phone: +86-10-62597285. Fax: +86-10-62597285.Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, ChinaMore by Pingli Dai,
- Zhenxiong Yan ,
- Shilong MaShilong MaKey Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, ChinaCollege of Bee Science, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaMore by Shilong Ma,
- Yang YangYang YangKey Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, ChinaMore by Yang Yang,
- Qiang WangQiang WangKey Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, ChinaMore by Qiang Wang,
- Chunsheng HouChunsheng HouKey Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, ChinaMore by Chunsheng Hou,
- Yanyan WuYanyan WuKey Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, ChinaMore by Yanyan Wu,
- Yongjun LiuYongjun LiuKey Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, ChinaMore by Yongjun Liu, and
- Qingyun Diao*Qingyun Diao*E-mail: [email protected]Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, ChinaMore by Qingyun Diao
Abstract

Effects of glyphosate on survival, developmental rate, larval weight, and midgut bacterial diversity of Apis mellifera were tested in the laboratory. Larvae were reared in vitro and fed diet containing glyphosate 0.8, 4, and 20 mg/L. The dependent variables were compared with negative control and positive control (dimethoate 45 mg/L). Brood survival decreased in 4 or 20 mg/L glyphosate treatments but not in 0.8 mg/L, and larval weight decreased in 0.8 or 4 mg/L glyphosate treatments. Exposure to three concentrations did not affect the developmental rate. Furthermore, the intestinal bacterial communities were determined using high-throughput sequencing targeting the V3–V4 regions of the 16S rDNA. All core honey bee intestinal bacterial phyla such as Proteobacteria (30.86%), Firmicutes (13.82%), and Actinobacteria (11.88%) were detected, and significant changes were found in the species diversity and richness in 20 mg/L glyphosate group. Our results suggest that high concentrations of glyphosate are deleterious to immature bees.
Cited By
This article is cited by 55 publications.
- Xueke Gao, Fangmei Hu, Shuai Zhang, Junyu Luo, Xiangzhen Zhu, Li Wang, Kaixin Zhang, Dongyang Li, Jichao Ji, Lin Niu, Changcai Wu, Jinjie Cui. Glyphosate exposure disturbs the bacterial endosymbiont community and reduces body weight of the predatory ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). Science of The Total Environment 2021, 790 , 147847. https://doi.org/10.1016/j.scitotenv.2021.147847
- Lucas Battisti, Michele Potrich, Amanda Roberta Sampaio, Nédia de Castilhos Ghisi, Fabiana Martins Costa-Maia, Raiza Abati, Claudia Bueno dos Reis Martinez, Silvia Helena Sofia. Response to Letter to the Editor “Is glyphosate toxic to bees? A meta-analytical review”. Science of The Total Environment 2021, 790 , 147517. https://doi.org/10.1016/j.scitotenv.2021.147517
- Caio Eduardo da Costa Domingues, Rafaela Tadei, Lais Vieira Bello Inoue, Elaine Cristina Mathias da Silva-Zacarin, Osmar Malaspina. Effects of larval exposure to the fungicide pyraclostrobin on the post-embryonic development of Africanized Apis mellifera workers. Environmental Advances 2021, 4 , 100069. https://doi.org/10.1016/j.envadv.2021.100069
- Carolyn A. Sonter, Romina Rader, Gavin Stevenson, Jamie R. Stavert, Susan C. Wilson. Biological and behavioral responses of European honey bee ( Apis mellifera ) colonies to perfluorooctane sulfonate exposure. Integrated Environmental Assessment and Management 2021, 17 (4) , 673-683. https://doi.org/10.1002/ieam.4421
- Scott F. Gilbert. Evolutionary developmental biology and sustainability: A biology of resilience. Evolution & Development 2021, 23 (4) , 273-291. https://doi.org/10.1111/ede.12366
- Anita Giglio, Maria Luigia Vommaro, Fabrizia Gionechetti, Alberto Pallavicini. Gut microbial community response to herbicide exposure in a ground beetle. Journal of Applied Entomology 2021, 26 https://doi.org/10.1111/jen.12919
- Gurleen Kaur, Rohit Sharma, Ashun Chaudhary, Randeep Singh. Factors Affecting Immune Responses in Honey Bees: An Insight. Journal of Apicultural Science 2021, 65 (1) , 25-47. https://doi.org/10.2478/jas-2021-0012
- Lucas Battisti, Michele Potrich, Amanda Roberta Sampaio, Nédia de Castilhos Ghisi, Fabiana Martins Costa-Maia, Raiza Abati, Claudia Bueno dos Reis Martinez, Silvia Helena Sofia. Is glyphosate toxic to bees? A meta-analytical review. Science of The Total Environment 2021, 767 , 145397. https://doi.org/10.1016/j.scitotenv.2021.145397
- Shilong Ma, Yang Yang, Zhongmin Fu, Qingyun Diao, Mengyue Wang, Qihua Luo, Xing Wang, Pingli Dai. A combination of Tropilaelaps mercedesae and imidacloprid negatively affects survival, pollen consumption and midgut bacterial composition of honey bee. Chemosphere 2021, 268 , 129368. https://doi.org/10.1016/j.chemosphere.2020.129368
- C. Orso, T.B. Stefanello, C.H. Franceschi, M.B. Mann, A.P.M. Varela, I.M.S. Castro, J. Frazzon, A.P.G. Frazzon, I. Andretta, A.M.L. Ribeiro. Changes in the ceca microbiota of broilers vaccinated for coccidiosis or supplemented with salinomycin. Poultry Science 2021, 100 (4) , 100969. https://doi.org/10.1016/j.psj.2020.12.066
- Gigi Davidson. Honey Bee Pharmacology. 2021,,, 135-148. https://doi.org/10.1002/9781119583417.ch10
- Sofia Graffigna, Hugo J. Marrero, Juan P. Torretta. Glyphosate commercial formulation negatively affects the reproductive success of solitary wild bees in a Pampean agroecosystem. Apidologie 2021, 52 (1) , 272-281. https://doi.org/10.1007/s13592-020-00816-8
- Ivana N. Macri, Diego E. Vázquez, Eduardo A. Pagano, Jorge A. Zavala, Walter M. Farina. Evaluating the Impact of Post-Emergence Weed Control in Honeybee Colonies Located in Different Agricultural Surroundings. Insects 2021, 12 (2) , 163. https://doi.org/10.3390/insects12020163
- Sheldon Krimsky. Can Glyphosate-Based Herbicides Contribute to Sustainable Agriculture?. Sustainability 2021, 13 (4) , 2337. https://doi.org/10.3390/su13042337
- Man-Hong Ye, Shu-Hang Fan, Xiao-Yuan Li, Islam Mohd Tarequl, Chun-Xiang Yan, Wan-Hong Wei, Sheng-Mei Yang, Bin Zhou. Microbiota dysbiosis in honeybee ( Apis mellifera L . ) larvae infected with brood diseases and foraging bees exposed to agrochemicals. Royal Society Open Science 2021, 8 (1) , 201805. https://doi.org/10.1098/rsos.201805
- Yueyue Liu, Chen Wang, Suzhen Qi, Jiang He, Yingchen Bai. The sublethal effects of ethiprole on the development, defense mechanisms, and immune pathways of honeybees (Apis mellifera L.). Environmental Geochemistry and Health 2021, 43 (1) , 461-473. https://doi.org/10.1007/s10653-020-00736-7
- Jingliang Shi, Ruonan Zhang, Yalin Pei, Chunhua Liao, Xiaobo Wu. Exposure to acetamiprid influences the development and survival ability of worker bees (Apis mellifera L.) from larvae to adults. Environmental Pollution 2020, 266 , 115345. https://doi.org/10.1016/j.envpol.2020.115345
- Hang Zhao, Guilin Li, Dezheng Guo, Ying Wang, Qingxin Liu, Zheng Gao, Hongfang Wang, Zhenguo Liu, Xingqi Guo, Baohua Xu. Transcriptomic and metabolomic landscape of the molecular effects of glyphosate commercial formulation on Apis mellifera ligustica and Apis cerana cerana. Science of The Total Environment 2020, 744 , 140819. https://doi.org/10.1016/j.scitotenv.2020.140819
- Martin Šlachta, Tomáš Erban, Alena Votavová, Tomáš Bešta, Michal Skalský, Marta Václavíková, Taťána Halešová, Magda Edwards-Jonášová, Renata Včeláková, Pavel Cudlín. Domestic Gardens Mitigate Risk of Exposure of Pollinators to Pesticides—An Urban-Rural Case Study Using a Red Mason Bee Species for Biomonitoring. Sustainability 2020, 12 (22) , 9427. https://doi.org/10.3390/su12229427
- Zhi-Wen Luo, Zhi-Xiang Dong, Yi-Fei Chen, Huan-Yuan Li, Qi-He Tang, Ji-Lian Li, Jun Guo. Comparative analysis of the gut microbiota of Apis cerana in Yunnan using high-throughput sequencing. Archives of Microbiology 2020, 202 (9) , 2557-2567. https://doi.org/10.1007/s00203-020-01974-0
- Sahar Delkash-Roudsari, Ana M. Chicas-Mosier, Seyed Hossein Goldansaz, Khalil Talebi-Jahromi, Ahmad Ashouri, Charles I. Abramson. Assessment of lethal and sublethal effects of imidacloprid, ethion, and glyphosate on aversive conditioning, motility, and lifespan in honey bees (Apis mellifera L.). Ecotoxicology and Environmental Safety 2020, 204 , 111108. https://doi.org/10.1016/j.ecoenv.2020.111108
- Elena Zioga, Ruth Kelly, Blánaid White, Jane C. Stout. Plant protection product residues in plant pollen and nectar: A review of current knowledge. Environmental Research 2020, 189 , 109873. https://doi.org/10.1016/j.envres.2020.109873
- Richard Odemer, Abdulrahim T. Alkassab, Gabriela Bischoff, Malte Frommberger, Anna Wernecke, Ina P. Wirtz, Jens Pistorius, Franziska Odemer. Chronic High Glyphosate Exposure Delays Individual Worker Bee (Apis mellifera L.) Development under Field Conditions. Insects 2020, 11 (10) , 664. https://doi.org/10.3390/insects11100664
- Erick V. S. Motta, Myra Mak, Tyler K. De Jong, J. Elijah Powell, Angela O'Donnell, Kristin J. Suhr, Ian M. Riddington, Nancy A. Moran, . Oral or Topical Exposure to Glyphosate in Herbicide Formulation Impacts the Gut Microbiota and Survival Rates of Honey Bees. Applied and Environmental Microbiology 2020, 86 (18) https://doi.org/10.1128/AEM.01150-20
- Erick V. S. Motta, Nancy A. Moran, . Impact of Glyphosate on the Honey Bee Gut Microbiota: Effects of Intensity, Duration, and Timing of Exposure. mSystems 2020, 5 (4) https://doi.org/10.1128/mSystems.00268-20
- Karen Chiu, Genoa Warner, Romana A Nowak, Jodi A Flaws, Wenyan Mei. The Impact of Environmental Chemicals on the Gut Microbiome. Toxicological Sciences 2020, 176 (2) , 253-284. https://doi.org/10.1093/toxsci/kfaa065
- Joseph Belsky, Neelendra K. Joshi. Effects of Fungicide and Herbicide Chemical Exposure on Apis and Non-Apis Bees in Agricultural Landscape. Frontiers in Environmental Science 2020, 8 https://doi.org/10.3389/fenvs.2020.00081
- Daria Sgargi, Balazs Adam, Lygia T. Budnik, Giovanni Dinelli, Horatiu Remus Moldovan, Melissa J. Perry, Paul TJ. Scheepers, Vivi Schlünssen, João Paulo Teixeira, Daniele Mandrioli, Fiorella Belpoggi. Protocol for a systematic review and meta-analysis of human exposure to pesticide residues in honey and other bees’ products. Environmental Research 2020, 186 , 109470. https://doi.org/10.1016/j.envres.2020.109470
- Christopher A. Halsch, Aimee Code, Sarah M. Hoyle, James A. Fordyce, Nicolas Baert, Matthew L. Forister. Pesticide Contamination of Milkweeds Across the Agricultural, Urban, and Open Spaces of Low-Elevation Northern California. Frontiers in Ecology and Evolution 2020, 8 https://doi.org/10.3389/fevo.2020.00162
- Diego E. Vázquez, José M. Latorre-Estivalis, Sheila Ons, Walter M. Farina. Chronic exposure to glyphosate induces transcriptional changes in honey bee larva: A toxicogenomic study. Environmental Pollution 2020, 261 , 114148. https://doi.org/10.1016/j.envpol.2020.114148
- Gyan P. Harwood, Adam G. Dolezal. Pesticide–Virus Interactions in Honey Bees: Challenges and Opportunities for Understanding Drivers of Bee Declines. Viruses 2020, 12 (5) , 566. https://doi.org/10.3390/v12050566
- Rebecca Mackelprang, Peggy G. Lemaux. Genetic Engineering and Editing of Plants: An Analysis of New and Persisting Questions. Annual Review of Plant Biology 2020, 71 (1) , 659-687. https://doi.org/10.1146/annurev-arplant-081519-035916
- Katarina Fritz‐Wallace, Beatrice Engelmann, Jannike L. Krause, Stephanie S. Schäpe, Judith Pöppe, Gunda Herberth, Uwe Rösler, Nico Jehmlich, Martin Bergen, Ulrike Rolle‐Kampczyk. Quantification of glyphosate and aminomethylphosphonic acid from microbiome reactor fluids. Rapid Communications in Mass Spectrometry 2020, 34 (7) https://doi.org/10.1002/rcm.8668
- Yang Yang, Shilong Ma, Feng Liu, Qiang Wang, Xing Wang, Chunsheng Hou, Yanyan Wu, Jing Gao, Li Zhang, Yongjun Liu, Qingyun Diao, Pingli Dai. Acute and chronic toxicity of acetamiprid, carbaryl, cypermethrin and deltamethrin to Apis mellifera larvae reared in vitro. Pest Management Science 2020, 76 (3) , 978-985. https://doi.org/10.1002/ps.5606
- Suzhen Qi, Lizhen Zhu, Donghui Wang, Chen Wang, Xiaofeng Chen, Xiaofeng Xue, Liming Wu. Flumethrin at honey-relevant levels induces physiological stresses to honey bee larvae (Apis mellifera L.) in vitro. Ecotoxicology and Environmental Safety 2020, 190 , 110101. https://doi.org/10.1016/j.ecoenv.2019.110101
- Lizhen Zhu, Suzhen Qi, Xiaofeng Xue, Xinyue Niu, Liming Wu. Nitenpyram disturbs gut microbiota and influences metabolic homeostasis and immunity in honey bee (Apis mellifera L.). Environmental Pollution 2020, 258 , 113671. https://doi.org/10.1016/j.envpol.2019.113671
- S. Iori, G. Dalla Rovere, L. Ezzat, M. Smits, S.S. Ferraresso, M. Babbucci, M.G. Marin, L. Masiero, J. Fabrello, E. Garro, L. Carraro, B. Cardazzo, T. Patarnello, V. Matozzo, L. Bargelloni, M. Milan. The effects of glyphosate and AMPA on the mediterranean mussel Mytilus galloprovincialis and its microbiota. Environmental Research 2020, 182 , 108984. https://doi.org/10.1016/j.envres.2019.108984
- Michelle L. Ledoux, Navam Hettiarachchy, Xiaofan Yu, Luke Howard, Sun-Ok Lee. Penetration of glyphosate into the food supply and the incidental impact on the honey supply and bees. Food Control 2020, 109 , 106859. https://doi.org/10.1016/j.foodcont.2019.106859
- Mikhail Y. Syromyatnikov, Mariya M. Isuwa, Olga V. Savinkova, Mariya I. Derevshchikova, Vasily N. Popov. The Effect of Pesticides on the Microbiome of Animals. Agriculture 2020, 10 (3) , 79. https://doi.org/10.3390/agriculture10030079
- John A. Chmiel, Brendan A. Daisley, Andrew P. Pitek, Graham J. Thompson, Gregor Reid. Understanding the Effects of Sublethal Pesticide Exposure on Honey Bees: A Role for Probiotics as Mediators of Environmental Stress. Frontiers in Ecology and Evolution 2020, 8 https://doi.org/10.3389/fevo.2020.00022
- Marwa M. El-Dalatony, Xiangkai Li. Environmental Pollutants That Can Be Metabolized by the Host (Gut Microbiota). 2020,,, 145-168. https://doi.org/10.1007/978-981-15-4759-1_5
- Suzhen Qi, Xinyue Niu, Dong hui Wang, Chen Wang, Lizhen Zhu, Xiaofeng Xue, Zhongyin Zhang, Liming Wu. Flumethrin at sublethal concentrations induces stresses in adult honey bees (Apis mellifera L.). Science of The Total Environment 2020, 700 , 134500. https://doi.org/10.1016/j.scitotenv.2019.134500
- Merissa G. Cullen, Linzi J. Thompson, James. C. Carolan, Jane C. Stout, Dara A. Stanley, . Fungicides, herbicides and bees: A systematic review of existing research and methods. PLOS ONE 2019, 14 (12) , e0225743. https://doi.org/10.1371/journal.pone.0225743
- Joseph L. Dempsey, Mallory Little, Julia Yue Cui. Gut microbiome: An intermediary to neurotoxicity. NeuroToxicology 2019, 75 , 41-69. https://doi.org/10.1016/j.neuro.2019.08.005
- Yahya Al Naggar, Boris Baer. Consequences of a short time exposure to a sublethal dose of Flupyradifurone (Sivanto) pesticide early in life on survival and immunity in the honeybee (Apis mellifera). Scientific Reports 2019, 9 (1) https://doi.org/10.1038/s41598-019-56224-1
- L.L. Botina, M. Vélez, W.F. Barbosa, A.C. Mendonça, V.S. Pylro, M.R. Tótola, G.F. Martins. Behavior and gut bacteria of Partamona helleri under sublethal exposure to a bioinsecticide and a leaf fertilizer. Chemosphere 2019, 234 , 187-195. https://doi.org/10.1016/j.chemosphere.2019.06.048
- Walter M. Farina, M. Sol Balbuena, Lucila T. Herbert, Carolina Mengoni Goñalons, Diego E. Vázquez. Effects of the Herbicide Glyphosate on Honey Bee Sensory and Cognitive Abilities: Individual Impairments with Implications for the Hive. Insects 2019, 10 (10) , 354. https://doi.org/10.3390/insects10100354
- Julie Dechartres, Jodi L. Pawluski, Marie‐Madeleine Gueguen, Amin Jablaoui, Emmanuelle Maguin, Moez Rhimi, Thierry D. Charlier. Glyphosate and glyphosate‐based herbicide exposure during the peripartum period affects maternal brain plasticity, maternal behaviour and microbiome. Journal of Neuroendocrinology 2019, 31 (9) https://doi.org/10.1111/jne.12731
- Xianling Yuan, Zihong Pan, Cuiyuan Jin, Yinhua Ni, Zhengwei Fu, Yuanxiang Jin. Gut microbiota: An underestimated and unintended recipient for pesticide-induced toxicity. Chemosphere 2019, 227 , 425-434. https://doi.org/10.1016/j.chemosphere.2019.04.088
- Yang Yang, Shilong Ma, Zhenxiong Yan, Feng Liu, Qingyun Diao, Pingli Dai. Effects of three common pesticides on survival, food consumption and midgut bacterial communities of adult workers Apis cerana and Apis mellifera. Environmental Pollution 2019, 249 , 860-867. https://doi.org/10.1016/j.envpol.2019.03.077
- Nicolas Blot, Loïs Veillat, Régis Rouzé, Hélène Delatte, . Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota. PLOS ONE 2019, 14 (4) , e0215466. https://doi.org/10.1371/journal.pone.0215466
- Douglas B. Sponsler, Christina M. Grozinger, Claudia Hitaj, Maj Rundlöf, Cristina Botías, Aimee Code, Eric V. Lonsdorf, Andony P. Melathopoulos, David J. Smith, Sainath Suryanarayanan, Wayne E. Thogmartin, Neal M. Williams, Minghua Zhang, Margaret R. Douglas. Pesticides and pollinators: A socioecological synthesis. Science of The Total Environment 2019, 662 , 1012-1027. https://doi.org/10.1016/j.scitotenv.2019.01.016
- Angelika Hilbeck, Nicolas Defarge, Thomas Bøhn, Michelle Krautter, Constanze Conradin, Caroline Amiel, Jean-Michel Panoff, Miluse Trtikova. Impact of Antibiotics on Efficacy of Cry Toxins Produced in Two Different Genetically Modified Bt Maize Varieties in Two Lepidopteran Herbivore Species, Ostrinia nubilalis and Spodoptera littoralis. Toxins 2018, 10 (12) , 489. https://doi.org/10.3390/toxins10120489
- Diego E. Vázquez, Natalia Ilina, Eduardo A. Pagano, Jorge A. Zavala, Walter M. Farina, . Glyphosate affects the larval development of honey bees depending on the susceptibility of colonies. PLOS ONE 2018, 13 (10) , e0205074. https://doi.org/10.1371/journal.pone.0205074
- Hector R. Valenzuela. Pollinators and Sustainable Farming in Hawaii. Bee World 2018, 95 (4) , 117-121. https://doi.org/10.1080/0005772X.2018.1507347




