ACS Publications. Most Trusted. Most Cited. Most Read
The Herbicide Glyphosate Negatively Affects Midgut Bacterial Communities and Survival of Honey Bee during Larvae Reared in Vitro

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Agric. Food Chem. 2018, 66, 29, 7786-7793
    Article

    The Herbicide Glyphosate Negatively Affects Midgut Bacterial Communities and Survival of Honey Bee during Larvae Reared in Vitro
    Click to copy article linkArticle link copied!

    • Pingli Dai*
      Pingli Dai
      Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
      *E-mail: [email protected]. Phone: +86-10-62597285. Fax: +86-10-62597285.
      More by Pingli Dai
      Orcidhttp://orcid.org/0000-0002-8297-652X
    • Zhenxiong Yan
      Zhenxiong Yan
      Beijing University of Agriculture, Beijing 102206, China
      More by Zhenxiong Yan
    • Shilong Ma
      Shilong Ma
      Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
      College of Bee Science, Fujian Agriculture and Forestry University, Fuzhou 350002, China
      More by Shilong Ma
    • Yang Yang
      Yang Yang
      Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
      More by Yang Yang
    • Qiang Wang
      Qiang Wang
      Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
      More by Qiang Wang
    • Chunsheng Hou
      Chunsheng Hou
      Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
      More by Chunsheng Hou
    • Yanyan Wu
      Yanyan Wu
      Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
      More by Yanyan Wu
    • Yongjun Liu
      Yongjun Liu
      Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
      More by Yongjun Liu
    • Qingyun Diao*
      Qingyun Diao
      Key Laboratory of Pollinating Insect Biology, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
      *E-mail: [email protected]
      More by Qingyun Diao
    Other Access OptionsSupporting Information (1)

    Journal of Agricultural and Food Chemistry

    Cite this: J. Agric. Food Chem. 2018, 66, 29, 7786–7793
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jafc.8b02212
    Published July 11, 2018
    Copyright © 2018 American Chemical Society
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    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.

    Copyright © 2018 American Chemical Society

    Subjects

    what are subjects

    Keywords

    what are keywords

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.8b02212.

    • OTUs and sequence read number; larval development rate, pupal development rate, and both combined (total) rate of honey bees reared in vitro and exposed to exposed to glyphosate in diet on D2 thru D5 after grafting (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai
    powered by  Scite

    This article is cited by 127 publications.

    1. Rita Végh, Csilla Sörös, Nándor Majercsik, László Sipos. Determination of Pesticides in Bee Pollen: Validation of a Multiresidue High-Performance Liquid Chromatography-Mass Spectrometry/Mass Spectrometry Method and Testing Pollen Samples of Selected Botanical Origin. Journal of Agricultural and Food Chemistry 2022, 70 (5) , 1507-1515. https://doi.org/10.1021/acs.jafc.1c06864
    2. Agnieszka Murawska, Ewelina Berbeć, Krzysztof Latarowski, Adam Roman, Paweł Migdał, . Semi-field studies on biochemical markers of honey bee workers (Apis mellifera) after exposure to pesticides and their mixtures. PLOS ONE 2025, 20 (1) , e0309567. https://doi.org/10.1371/journal.pone.0309567
    3. P. Basu, H.T. Ngo, M.A. Aizen, L.A. Garibaldi, B. Gemmill-Herren, V. Imperatriz-Fonseca, A.M. Klein, S.G. Potts, C.L. Seymour, A.J. Vanbergen. Pesticide impacts on insect pollinators: Current knowledge and future research challenges. Science of The Total Environment 2024, 954 , 176656. https://doi.org/10.1016/j.scitotenv.2024.176656
    4. Yuchen Su, Jingliang Shi, Yueyang Hu, Jianhui Liu, Xiaobo Wu. Acetamiprid Exposure Disrupts Gut Microbiota in Adult and Larval Worker Honeybees (Apis mellifera L.). Insects 2024, 15 (12) , 927. https://doi.org/10.3390/insects15120927
    5. Małgorzata Baćmaga, Jadwiga Wyszkowska, Jan Kucharski. Environmental Implication of Herbicide Use. Molecules 2024, 29 (24) , 5965. https://doi.org/10.3390/molecules29245965
    6. Diego E. Vázquez, Facundo Verellen, Walter M. Farina. Early exposure to glyphosate during larval development induces late behavioural effects on adult honey bees. Environmental Pollution 2024, 360 , 124674. https://doi.org/10.1016/j.envpol.2024.124674
    7. Carmen A. Nebauer, Paula Prucker, Fabian A. Ruedenauer, Johannes Kollmann, Sara D. Leonhardt. Bumblebees under stress: Interacting effects of pesticides and heatwaves on colony development and longevity. iScience 2024, 27 (11) , 111050. https://doi.org/10.1016/j.isci.2024.111050
    8. Jiao Tang, Chenglin Chi, Jiaxing Huang, Guiling Ding. Development and applications of in vitro artificial rearing of honey bee larvae. Journal of Apicultural Research 2024, 58 , 1-15. https://doi.org/10.1080/00218839.2024.2412437
    9. Erick V. S. Motta, Tyler K. de Jong, Alejandra Gage, Joseph A. Edwards, Nancy A. Moran, . Glyphosate effects on growth and biofilm formation in bee gut symbionts and diverse associated bacteria. Applied and Environmental Microbiology 2024, 90 (8) https://doi.org/10.1128/aem.00515-24
    10. Bin Li, Xiasang Chen, Li Ke, Pingli Dai, Yuan Ge, Yong-Jun Liu. Early-Life Sublethal Exposure to Thiacloprid Alters Adult Honeybee Gut Microbiota. Genes 2024, 15 (8) , 1001. https://doi.org/10.3390/genes15081001
    11. Amanda da Cunha Ignácio, Andressa Maria dos Reis Guerra, Thaiany Goulart de Souza-Silva, Mariana Araújo Vieira do Carmo, Hudsara Aparecida de Almeida Paula. Effects of glyphosate exposure on intestinal microbiota, metabolism and microstructure: a systematic review. Food & Function 2024, 15 (15) , 7757-7781. https://doi.org/10.1039/D4FO00660G
    12. Shiqi Luo, Xue Zhang, Xin Zhou. Temporospatial dynamics and host specificity of honeybee gut bacteria. Cell Reports 2024, 43 (7) , 114408. https://doi.org/10.1016/j.celrep.2024.114408
    13. Laina Pires Rosa, Marcela Cristina A. C. Silveira-Tschoeke, Carlos Gravato, Pedro Henrique O. Lima, Ana M. Cezario, Paulo Henrique Tschoeke, Renato Almeida Sarmento. Does roundup® affect worker bees ( Apis mellifera ) that inhabit areas of high agrochemical pressure?. Journal of Apicultural Research 2024, 7 , 1-11. https://doi.org/10.1080/00218839.2024.2361940
    14. Shing Ching Khoo, Nan Zhang, Vijitra Luang-In, Meng Shien Goh, Christian Sonne, Nyuk Ling Ma. Exploring environmental exposomes and the gut-brain nexus: Unveiling the impact of pesticide exposure. Environmental Research 2024, 250 , 118441. https://doi.org/10.1016/j.envres.2024.118441
    15. Changsheng Ma, Gaoying Gu, Sihao Chen, Xiaoyu Shi, Zuren Li, Hongmei Li-Byarlay, Lianyang Bai. Impact of chronic exposure to field level glyphosate on the food consumption, survival, gene expression, gut microbiota, and metabolomic profiles of honeybees. Environmental Research 2024, 250 , 118509. https://doi.org/10.1016/j.envres.2024.118509
    16. Yuxin Kang, Tong Wu, Bo Han, Sa Yang, Xing Wang, Qiang Wang, Jing Gao, Pingli Dai. Interaction of acetamiprid, Varroa destructor, and Nosema ceranae in honey bees. Journal of Hazardous Materials 2024, 471 , 134380. https://doi.org/10.1016/j.jhazmat.2024.134380
    17. Liyaqat Ayoub, Munazah Yaqoob, Raihana H. Kanth, Fehim Jeelani Wani, Fazil Fayaz Wani, Audil Gull. Comparative Acute Toxicity and Safety Indices of Organophosphate Insecticides on Apis mellifera. 2024https://doi.org/10.21203/rs.3.rs-4411141/v1
    18. Yali Du, Kai Xu, Huiting Zhao, Ying Wu, Haibin Jiang, Jinming He, Yusuo Jiang. Preliminary Study on the Pathogenic Mechanism of Jujube Flower Disease in Honeybees (Apis mellifera ligustica) Based on Midgut Transcriptomics. Genes 2024, 15 (5) , 533. https://doi.org/10.3390/genes15050533
    19. Zhong-di HUANG, Shu-ping SHI, Yi ZHANG, Cai-ping YIN, Shu-xiang ZHANG, Yinglao Zhang. Isolation, Characterization, and Herbicidal Activity of Streptomyces spp. from Diseased Potato Scab Tubers. 2024https://doi.org/10.21203/rs.3.rs-3991115/v1
    20. Thierry D. Charlier. Impact de l’exposition au glyphosate sur la neuroplasticité – de la mère à la descendance. Cahiers de Nutrition et de Diététique 2024, 59 (2) , 128-139. https://doi.org/10.1016/j.cnd.2023.12.006
    21. Erick V. S. Motta, Tyler K. de Jong, Alejandra Gage, Joseph A. Edwards, Nancy A. Moran. Glyphosate Effects on Growth and Biofilm Formation in Bee Gut Symbionts and Diverse Associated Bacteria. 2024https://doi.org/10.1101/2024.03.20.585985
    22. Zhi Li, Yuedi Wang, Qiqian Qin, Lanchun Chen, Xiaoqun Dang, Zhengang Ma, Zeyang Zhou. Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera. eLife 2024, 12 https://doi.org/10.7554/eLife.88772
    23. Zhi Li, Yuedi Wang, Qiqian Qin, Lanchun Chen, Xiaoqun Dang, Zhengang Ma, Zeyang Zhou. Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera. eLife 2024, 12 https://doi.org/10.7554/eLife.88772.4
    24. Michelle Z. Hotchkiss, Jessica R. K. Forrest, Alexandre J. Poulain, . Exposure to a fungicide for a field-realistic duration does not alter bumble bee fecal microbiota structure. Applied and Environmental Microbiology 2024, 90 (2) https://doi.org/10.1128/aem.01739-23
    25. Zhi Li, Yuedi Wang, Qiqian Qin, Lanchun Chen, Xiaoqun Dang, Zhengang Ma, Zeyang Zhou. Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera. 2024https://doi.org/10.7554/eLife.88772.3
    26. Yahya Al Naggar, Tesfaye Wubet. Chronic exposure to pesticides disrupts the bacterial and fungal co-existence and the cross-kingdom network characteristics of honey bee gut microbiome. Science of The Total Environment 2024, 906 , 167530. https://doi.org/10.1016/j.scitotenv.2023.167530
    27. Xueke Gao, Fangmei Hu, Huanfei Cui, Xiangzhen Zhu, Li Wang, Kaixin Zhang, Dongyang Li, Jichao Ji, Junyu Luo, Jinjie Cui. Glyphosate decreases survival, increases fecundity, and alters the microbiome of the natural predator Harmonia axyridis (ladybird beetle). Environmental Research 2023, 238 , 117174. https://doi.org/10.1016/j.envres.2023.117174
    28. Edward A. Straw, Robin Mesnage, Mark J. F. Brown, Michael N. Antoniou. No impacts of glyphosate or Crithidia bombi, or their combination, on the bumblebee microbiome. Scientific Reports 2023, 13 (1) https://doi.org/10.1038/s41598-023-35304-3
    29. Mohammad Abdul Waseem, Meena Thakur. Toxicity of Insecticides with Different Modes of Action to Apis Mellifera Larvae (Hymenoptera, Apidae). Journal of Apicultural Science 2023, 67 (2) , 115-123. https://doi.org/10.2478/jas-2023-0010
    30. Qibao He, Shiyu Zhang, Fang Yin, Qiongqiong Liu, Quan Gao, Jinjing Xiao, Yong Huang, Linsheng Yu, Haiqun Cao. Risk assessment of honeybee larvae exposure to pyrethroid insecticides in beebread and honey. Ecotoxicology and Environmental Safety 2023, 267 , 115591. https://doi.org/10.1016/j.ecoenv.2023.115591
    31. Renan dos Santos Araújo, Thaís Andrade Viana, Lorena Lisbetd Botina, Daniel Silva Sena Bastos, Beatriz Cristina da Silva Alves, Mariana Machado-Neves, Rodrigo Cupertino Bernardes, Gustavo Ferreira Martins. Investigating the effects of mesotrione/atrazine-based herbicide on honey bee foragers. Science of The Total Environment 2023, 898 , 165526. https://doi.org/10.1016/j.scitotenv.2023.165526
    32. Kai Han, Hongfang Wang, Zhenguo Liu, Xuepeng Chi, Ying Wang, Xuepei Cui, Baohua Xu. A study about the application of probiotics on Apis mellifera. Journal of Apicultural Research 2023, 62 (5) , 1070-1081. https://doi.org/10.1080/00218839.2022.2088933
    33. Álvaro Urueña, Nuria Blasco-Lavilla, Pilar De la Rúa. Sulfoxaflor effects depend on the interaction with other pesticides and Nosema ceranae infection in the honey bee (Apis mellifera). Ecotoxicology and Environmental Safety 2023, 264 , 115427. https://doi.org/10.1016/j.ecoenv.2023.115427
    34. Diego E. Vázquez, Luis E. Villegas Martínez, Virginia Medina, Jose M. Latorre-Estivalis, Jorge A. Zavala, Walter M. Farina. Glyphosate affects larval gut microbiota and metamorphosis of honey bees with differences between rearing procedures. Environmental Pollution 2023, 334 , 122200. https://doi.org/10.1016/j.envpol.2023.122200
    35. Christina Tsadila, Chiara Amoroso, Dimitris Mossialos. Microbial Diversity in Bee Species and Bee Products: Pseudomonads Contribution to Bee Well-Being and the Biological Activity Exerted by Honey Bee Products: A Narrative Review. Diversity 2023, 15 (10) , 1088. https://doi.org/10.3390/d15101088
    36. Zhi Li, Yuedi Wang, Qiqian Qin, Lanchun Chen, Xiaoqun Dang, Zhengang Ma, Zeyang Zhou. Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera. 2023https://doi.org/10.7554/eLife.88772.2
    37. Ingrid N. Gomes, Lessando Moreira Gontijo, Maria Augusta Pereira Lima, José Salazar Zanuncio, Helder Canto Resende. The survival and flight capacity of commercial honeybees and endangered stingless bees are impaired by common agrochemicals. Ecotoxicology 2023, 32 (7) , 937-947. https://doi.org/10.1007/s10646-023-02699-8
    38. Guofeng Chang, Hui Xue, Jichao Ji, Li Wang, Xiangzhen Zhu, Kaixin Zhang, Dongyang Li, Xueke Gao, Lin Niu, Mengxue Gao, Junyu Luo, Jinjie Cui. Risk assessment of predatory lady beetle Propylea japonica's multi-generational exposure to three non-insecticidal agrochemicals. Science of The Total Environment 2023, 886 , 163931. https://doi.org/10.1016/j.scitotenv.2023.163931
    39. Rie Matsuzaki, Eoin Gunnigle, Violette Geissen, Gerard Clarke, Jatin Nagpal, John F Cryan. Pesticide exposure and the microbiota-gut-brain axis. The ISME Journal 2023, 17 (8) , 1153-1166. https://doi.org/10.1038/s41396-023-01450-9
    40. Heather Patterson, Ella Bowles, Susan Chiblow, Deborah McGregor, Cory Kozmik, Jesse Popp. Environmental and socio-cultural impacts of glyphosate-based herbicides: perspectives from indigenous knowledge and western science. Frontiers in Conservation Science 2023, 4 https://doi.org/10.3389/fcosc.2023.1186399
    41. Zhi Li, Yuedi Wang, Qiqian Qin, Lanchun Chen, Xiaoqun Dang, Zhengang Ma, Zeyang Zhou. Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera. 2023https://doi.org/10.7554/eLife.88772.1
    42. Marjo Helander, Aditya Jeevannavar, Kimmo Kaakinen, Suni A Mathew, Kari Saikkonen, Benjamin Fuchs, Pere Puigbò, Olli J Loukola, Manu Tamminen. Glyphosate and a glyphosate-based herbicide affect bumblebee gut microbiota. FEMS Microbiology Ecology 2023, 99 (7) https://doi.org/10.1093/femsec/fiad065
    43. Aneta Bokšová, Jan Kazda, Jan Bartoška, Martin Kamler. Effect of glyphosate on the foraging activity of European honey bees (Apis mellifera L.). Plant, Soil and Environment 2023, 69 (5) , 195-201. https://doi.org/10.17221/86/2023-PSE
    44. Charlotte Steinigeweg, Abdulrahim T. Alkassab, Silvio Erler, Hannes Beims, Ina P. Wirtz, Dania Richter, Jens Pistorius. Impact of a Microbial Pest Control Product Containing Bacillus thuringiensis on Brood Development and Gut Microbiota of Apis mellifera Worker Honey Bees. Microbial Ecology 2023, 85 (4) , 1300-1307. https://doi.org/10.1007/s00248-022-02004-w
    45. Erick V.S. Motta, Nancy A. Moran. The effects of glyphosate, pure or in herbicide formulation, on bumble bees and their gut microbial communities. Science of The Total Environment 2023, 872 , 162102. https://doi.org/10.1016/j.scitotenv.2023.162102
    46. Yazi Li, Liyun Chang, Ke Xu, Shuhong Zhang, Fengju Gao, Yongshan Fan. Research Progresses on the Function and Detection Methods of Insect Gut Microbes. Microorganisms 2023, 11 (5) , 1208. https://doi.org/10.3390/microorganisms11051208
    47. Merissa G. Cullen, Liam Bliss, Dara A. Stanley, James C. Carolan. Investigating the effects of glyphosate on the bumblebee proteome and microbiota. Science of The Total Environment 2023, 864 , 161074. https://doi.org/10.1016/j.scitotenv.2022.161074
    48. N. Defarge, M. Otto, A. Hilbeck. A Roundup herbicide causes high mortality and impairs development of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). Science of The Total Environment 2023, 865 , 161158. https://doi.org/10.1016/j.scitotenv.2022.161158
    49. Manqiong Xiong, Gan Qin, Lizhu Wang, Ruyi Wang, Ruiqi Zhou, Xiaotian Luo, Qun Lou, Shaokang Huang, Jianghong Li, Xinle Duan. Field recommended concentrations of pyraclostrobin exposure disturb the development and immune response of worker bees (Apis mellifera L.) larvae and pupae. Frontiers in Physiology 2023, 14 https://doi.org/10.3389/fphys.2023.1137264
    50. Lucas Battisti, Michele Potrich, Everton Ricardi Lozano, Claudia Bueno dos Reis Martinez, Silvia Helena Sofia. Review on the sublethal effects of pure and formulated glyphosate on bees: Emphasis on social bees. Journal of Applied Entomology 2023, 147 (1) , 1-18. https://doi.org/10.1111/jen.13089
    51. Shenhang Cheng, Pingli Dai, Ren Li, Zhibin Chen, Pingzhuo Liang, Xiaoping Xie, Congai Zhen, Xiwu Gao. The sulfoximine insecticide sulfoxaflor exposure reduces the survival status and disrupts the intestinal metabolism of the honeybee Apis mellifera. Journal of Hazardous Materials 2023, 442 , 130109. https://doi.org/10.1016/j.jhazmat.2022.130109
    52. Beatriz Ibarra-Mendoza, Bruno Gomez-Gil, Miguel Betancourt-Lozano, Luciana Raggi, Beatriz Yáñez-Rivera. Microbial gut dysbiosis induced by xenobiotics in model organisms and the relevance of experimental criteria: a minireview. Gut Microbiome 2023, 4 https://doi.org/10.1017/gmb.2023.3
    53. Changsheng Ma, Gaoying Gu, Sihao Chen, Xiaoyu Shi, Zuren Li, Hongmei Li-Byarlay, Lianyang Bai. Impact of Glyphosate Application at the Field Level on Honeybee Food Consumption, Survival, Gene Expression, Gut Microbiota, and Metabolomic Profiles. 2023https://doi.org/10.2139/ssrn.4655448
    54. Anna Maria Campana, Hannah E. Laue, Yike Shen, Martha J. Shrubsole, Andrea A. Baccarelli. Assessing the role of the gut microbiome at the interface between environmental chemical exposures and human health: Current knowledge and challenges. Environmental Pollution 2022, 315 , 120380. https://doi.org/10.1016/j.envpol.2022.120380
    55. Hanine Almasri, Joanito Liberti, Jean-Luc Brunet, Philipp Engel, Luc P. Belzunces. Mild chronic exposure to pesticides alters physiological markers of honey bee health without perturbing the core gut microbiota. Scientific Reports 2022, 12 (1) https://doi.org/10.1038/s41598-022-08009-2
    56. Bo-Ram Yun, A-Tai Truong, Yong Soo Choi, Man Young Lee, Byoung Yong Kim, Minjung Seo, Soon-Seek Yoon, Mi-Sun Yoo, Dong Van Quyen, Yun Sang Cho. Comparison of the gut microbiome of sacbrood virus-resistant and -susceptible Apis cerana from South Korea. Scientific Reports 2022, 12 (1) https://doi.org/10.1038/s41598-022-13535-0
    57. Erick V. S. Motta, J. Elijah Powell, Nancy A. Moran. Glyphosate induces immune dysregulation in honey bees. Animal Microbiome 2022, 4 (1) https://doi.org/10.1186/s42523-022-00165-0
    58. D.L. Li, J.S. Wang, L.J. Liu, K. Li, Y.B. Xu, X.Q. Ding, Y.Y. Wang, Y.F. Zhang, L.Y. Xie, S. Liang, Y.X. Wang, X.A. Zhan. Effects of early post-hatch feeding on the growth performance, hormone secretion, intestinal morphology, and intestinal microbiota structure in broilers. Poultry Science 2022, 101 (11) , 102133. https://doi.org/10.1016/j.psj.2022.102133
    59. Yahya Al Naggar, Bala Singavarapu, Robert J. Paxton, Tesfaye Wubet. Bees under interactive stressors: the novel insecticides flupyradifurone and sulfoxaflor along with the fungicide azoxystrobin disrupt the gut microbiota of honey bees and increase opportunistic bacterial pathogens. Science of The Total Environment 2022, 849 , 157941. https://doi.org/10.1016/j.scitotenv.2022.157941
    60. Linzi J. Thompson, Stephen Smith, Jane C. Stout, Blánaid White, Elena Zioga, Dara A. Stanley. Bumblebees can be Exposed to the Herbicide Glyphosate when Foraging. Environmental Toxicology and Chemistry 2022, 41 (10) , 2603-2612. https://doi.org/10.1002/etc.5442
    61. Mirjalol Umurzokov, Youn-Me Lee, Hye Jin Kim, Kwang Min Cho, Young Sook Kim, Jung Sup Choi, Kee Woong Park. Herbicidal characteristics and structural identification of a potential active compound produced by Streptomyces sp. KRA18–249. Pesticide Biochemistry and Physiology 2022, 187 , 105213. https://doi.org/10.1016/j.pestbp.2022.105213
    62. Márton Papp, László Békési, Róbert Farkas, László Makrai, Maura Fiona Judge, Gergely Maróti, Dóra Tőzsér, Norbert Solymosi, . Natural diversity of the honey bee (Apis mellifera) gut bacteriome in various climatic and seasonal states. PLOS ONE 2022, 17 (9) , e0273844. https://doi.org/10.1371/journal.pone.0273844
    63. Pierre Antonelli, Pénélope Duval, Patricia Luis, Guillaume Minard, Claire Valiente Moro. Reciprocal interactions between anthropogenic stressors and insect microbiota. Environmental Science and Pollution Research 2022, 29 (43) , 64469-64488. https://doi.org/10.1007/s11356-022-21857-9
    64. Fangmei Hu, Lingen Du, Xueke Gao, Jinjie Cui, Xingmiao Zhou. Analysis of the bacterial communities of four predatory natural enemies collected from a Northern China Bt cotton field. Journal of Asia-Pacific Entomology 2022, 25 (3) , 101941. https://doi.org/10.1016/j.aspen.2022.101941
    65. Li Zhang, Feng Liu, Xin-Ling Wang, Pin-Hong Wang, Shi-Long Ma, Yang Yang, Wu-Guang Ye, Qing-Yun Diao, Ping-Li Dai. Midgut Bacterial Communities of Vespa velutina Lepeletier (Hymenoptera: Vespidae). Frontiers in Ecology and Evolution 2022, 10 https://doi.org/10.3389/fevo.2022.934054
    66. Tong Wu, Bo Han, Xing Wang, Yuemin Tong, Feng Liu, Qingyun Diao, Pingli Dai. Chlorothalonil alters the gut microbiota and reduces the survival of immature honey bees reared in vitro. Pest Management Science 2022, 78 (5) , 1976-1981. https://doi.org/10.1002/ps.6816
    67. Bin Li, Li Ke, Ai-Rui Li, Qing-Yun Diao, Qiang Wang, Yong-Jun Liu. Exposure of Larvae to Sublethal Thiacloprid Delays Bee Development and Affects Transcriptional Responses of Newly Emerged Honey Bees. Frontiers in Insect Science 2022, 2 https://doi.org/10.3389/finsc.2022.844957
    68. Michelle Z Hotchkiss, Alexandre J Poulain, Jessica R K Forrest. Pesticide-induced disturbances of bee gut microbiotas. FEMS Microbiology Reviews 2022, 46 (2) https://doi.org/10.1093/femsre/fuab056
    69. Sahar Delkash-Roudsari, Seyed Hossein Goldansaz, Khalil Talebi Jahromi, Ahmad Ashouri, Charles I. Abramson. Side effects of imidacloprid, ethion, and hexaflumuron on adult and larvae of honey bee Apis mellifera (Hymenoptera, Apidae). Apidologie 2022, 53 (1) https://doi.org/10.1007/s13592-022-00910-z
    70. Dalal M. Aljedani. Antibiotic treatment (Tetracycline) effect on bio-efficiency of the larvae honey bee (Apis mellifera jemenatica). Saudi Journal of Biological Sciences 2022, 29 (3) , 1477-1486. https://doi.org/10.1016/j.sjbs.2021.11.024
    71. Shuai Tan, Guilin Li, Zhenguo Liu, Hongfang Wang, Xingqi Guo, Baohua Xu. Effects of glyphosate exposure on honeybees. Environmental Toxicology and Pharmacology 2022, 90 , 103792. https://doi.org/10.1016/j.etap.2021.103792
    72. Evatt Chirgwin, Stuart Kemp, James L. Maino, Marielle Babineau, Isobel Roberts, Alana Govender, Paul A. Umina, . Beneficial invertebrates of dairy pastures in south-eastern Australia. Crop & Pasture Science 2022, 73 (6) , 716-731. https://doi.org/10.1071/CP21652
    73. Youn-Me Lee, Mirjalol Umurzokov, Hye Jin Kim, Kwang Min Cho, Young Sook Kim, Jung Sup Choi, Kee Woong Park. Herbicidal Characteristics and Structural Identification of the Potential Active Compounds from Streptomyces Sp. Kra18-249. SSRN Electronic Journal 2022, 223 https://doi.org/10.2139/ssrn.4141259
    74. Nicolas Defarge, Mathias Otto, Angelika Hilbeck. A Roundup Herbicide Causes High Mortality and Impairs Development of Chrysoperla Carnea (Stephens) (Neuroptera: Chrysopidae). SSRN Electronic Journal 2022, 44 https://doi.org/10.2139/ssrn.4172738
    75. 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, 145 (10) , 986-1000. https://doi.org/10.1111/jen.12919
    76. MINGKUI LV, QINGZHI LEI, HUAJUAN YIN, TIANNIAN HU, SIFAN WANG, KUN DONG, HONGBIN PAN, YIQIU LIU, QIUYE LIN, ZHENHUI CAO. In vitro Effects of Prebiotics and Synbiotics on Apis cerana Gut Microbiota. Polish Journal of Microbiology 2021, 70 (4) , 511-520. https://doi.org/10.33073/pjm-2021-049
    77. A. H. C. van Bruggen, M. R. Finckh, M. He, C. J. Ritsema, P. Harkes, D. Knuth, V. Geissen. Indirect Effects of the Herbicide Glyphosate on Plant, Animal and Human Health Through its Effects on Microbial Communities. Frontiers in Environmental Science 2021, 9 https://doi.org/10.3389/fenvs.2021.763917
    78. Jon Zawislak, Gus Lorenz, John Adamczyk, Robert Wiedenmann, Neelendra K. Joshi. Proportion of commodity crop pollens and pesticide contamination in honey bee diets in two different landscapes. Environmental Advances 2021, 5 , 100116. https://doi.org/10.1016/j.envadv.2021.100116
    79. 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
    80. 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
    81. 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
    82. 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
    83. 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
    84. 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
    85. 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
    86. 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
    87. 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
    88. Gigi Davidson. Honey Bee Pharmacology. 2021, 135-148. https://doi.org/10.1002/9781119583417.ch10
    89. 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
    90. 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
    91. Sheldon Krimsky. Can Glyphosate-Based Herbicides Contribute to Sustainable Agriculture?. Sustainability 2021, 13 (4) , 2337. https://doi.org/10.3390/su13042337
    92. 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
    93. Márton Papp, László Békési, Róbert Farkas, László Makrai, Gergely Maróti, Dóra Tőzsér, Norbert Solymosi. Natural diversity of honey bee ( Apis mellifera ) gut bacteriome in various climatic and seasonal states. 2021https://doi.org/10.1101/2021.01.27.428438
    94. Jose Luis Rodríguez-Gil, Ryan S. Prosser, Stephen O. Duke, Keith. R. Solomon. Ecotoxicology of Glyphosate, Its Formulants, and Environmental Degradation Products. 2021, 129-205. https://doi.org/10.1007/398_2020_56
    95. 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
    96. Edward A. Straw, Mark J.F. Brown. No evidence of effects or interaction between the widely used herbicide, glyphosate, and a common parasite in bumble bees. PeerJ 2021, 9 , e12486. https://doi.org/10.7717/peerj.12486
    97. 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
    98. 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
    99. 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
    100. 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
    Load all citations
    Download PDF
    Go to Journal of Agricultural and Food Chemistry
    Get e-Alerts
    Get e-Alerts

    Journal of Agricultural and Food Chemistry

    Cite this: J. Agric. Food Chem. 2018, 66, 29, 7786–7793
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jafc.8b02212
    Published July 11, 2018
    Copyright © 2018 American Chemical Society
    Request reuse permissions

    Article Views

    2567

    Altmetric

    -

    Citations

    127
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.