The honey bee gut microbiota: a review under the perspective of bees threatened by agrochemicals


  • Kilmer Oliveira Soares
  • Vanessa Luming Hale
  • Geovergue Rodrigues de Medeiros
  • Núbia Michelle Vieira da Silva
  • Marcos Venâncio Lima
  • Thamara Ferreira da Rocha
  • Patrício Borges Maracajá
  • Jose Henrique Souza Costa
  • Adriana Evangelista Rodrigues
  • Celso José Bruno de Oliveira



bees, intestines, microbiota, pesticides


Although it is very well known that bees play a key role in the stability of several ecosystems globally, anthropogenic activities causing environmental degradation, such as the use of agrochemicals, can ultimately lead to the extinction of native species, with severe ecological consequences. The advances in high throughput sequencing technologies and bioinformatics tools in the last decades have contributed to the understanding of the importance of the microbiome for the health of different animal species. However, there is a paucity of information on the effects of the exposition to agrochemicals on the microbial composition of honeybees and how this can compromise their health. In this systematic review article, we discuss the composition and biological function of native honeybee gut microbiota and how it can be possibly affected by agrochemicals, including antibiotics. We performed a systematic literature review focusing on the effect of agrochemical use on the gut microbiota of honey bees. A bibliographical survey was conducted from 1950 to 2023 in all available databases.  We used the keywords “honey bees”, “microbiome” and “agrochemicals”. A total of 95 papers addressing this topic were selected, carefully checked and grouped into three categories: 1) The bee microbiome and its importance; 2) Functional roles of the bee gut microbiome; and 3) The problem of the anthropic actions that threaten the gut microbiome of bees. The present report can serve future studies addressing the complex ecological aspects of antimicrobial usage in agriculture and livestock in the scope of honeybee preservation.


ALBUQUERQUE, Ulysses Paulino; GONÇALVES, Paulo Henrique Santos; FERREIRA JÚNIOR, Washington Soares; CHAVES, Leonardo Silva; OLIVEIRA, Regina Célia da Silva; SILVA, Temóteo Luiz Lima da; SANTOS, Gilney Charll dos; ARAÚJO, Elcida de Lima. Humans as niche constructors: Revisiting the concept of chronic anthropogenic disturbances in ecology. Perspectives in Ecology and Conservation, vol. 16, no. 1, p. 1–11, Jan. 2018.

ALCOCK, JOHN; BARROWS, EDWARD M.; GORDH, GORDON; HUBBARD, L. JAN; KIRKENDALL, LARRY; PYLE, DONALD W.; PONDER, TERRY L.; ZALOM, FRANK G. The ecology and evolution of male reproductive behaviour in the bees and wasps. Zoological Journal of the Linnean Society, vol. 64, no. 4, p. 293–326, Dec. 1978.

AL-KAHTANI, Saad N.; TAHA, El-Kazafy; KHAN, Khalid Ali; ANSARI, Mohammad Javed; FARAG, Soha A.; SHAWER, Dalia M. B.; ELNABAWY, El-Said Mohamed. Effect of harvest season on the nutritional value of bee pollen protein. PLOS ONE, vol. 15, no. 12, p. e0241393, 28 Dec. 2020.

ANDERSON, K. E.; SHEEHAN, T. H.; ECKHOLM, B. J.; MOTT, B. M.; DEGRANDI-HOFFMAN, G. An emerging paradigm of colony health: microbial balance of the honey bee and hive (Apis mellifera). Insectes Sociaux, vol. 58, no. 4, p. 431–444, 30 Nov. 2011.

BABAYEV, M. S.,; MAMEDOVA, R. F. Global problems of mankind. realities and prediction for the future. Journal of Agriculture and Environment, vol. 2, p. 6–6, 2019.

BALBUENA, Sofía; CASTELLI, Loreley; ZUNINO, Pablo; ANTÚNEZ, Karina. Effect of Chronic Exposure to Sublethal Doses of Imidacloprid and Nosema ceranae on Immunity, Gut Microbiota, and Survival of Africanized Honey Bees. Microbial Ecology, vol. 85, no. 4, p. 1485–1497, 23 May 2023.

BEUTLER, Ruth; OPFINGER, Elisabeth. Pollenernahrung und Nosemabefall der Honigbiene. Die Naturwissenschaften, vol. 35, no. 9, p. 288–288, 1948.

BLASER, Martin J. The microbiome revolution. Journal of Clinical Investigation, vol. 124, no. 10, p. 4162–4165, 1 Oct. 2014.

BOMFIM, I., Oliveira; M., & Freitas, B. Biologia das abelhas . FUNECE. Fortaleza: [s. n.], 2017. vol. 1, .

BORDIER, Célia; SUCHAIL, Séverine; PIOZ, Maryline; DEVAUD, Jean Marc; COLLET, Claude; CHARRETON, Mercedes; LE CONTE, Yves; ALAUX, Cédric. Stress response in honeybees is associated with changes in task-related physiology and energetic metabolism. Journal of Insect Physiology, vol. 98, p. 47–54, Apr. 2017.

BORRELY, Sueli Ivone; CAMINADA, Suzete Maria L.; PONEZI, Alexandre Nunes; SANTOS, Dymes Rafael; SILVA, Vanessa H. Ogihara. Contaminação das águas por resíduos de medicamentos: ênfase ao cloridrato de fluoxetina. O Mundo da Saúde, vol. 36, no. 4, p. 556–563, 30 Dec. 2012.

BRANSTETTER, Michael G.; DANFORTH, Bryan N.; PITTS, James P.; FAIRCLOTH, Brant C.; WARD, Philip S.; BUFFINGTON, Matthew L.; GATES, Michael W.; KULA, Robert R.; BRADY, Seán G. Phylogenomic Insights into the Evolution of Stinging Wasps and the Origins of Ants and Bees. Current Biology, vol. 27, no. 7, p. 1019–1025, Apr. 2017.

BREEZE, T.D.; BAILEY, A.P.; BALCOMBE, K.G.; POTTS, S.G. Pollination services in the UK: How important are honeybees? Agriculture, Ecosystems & Environment, vol. 142, no. 3–4, p. 137–143, Aug. 2011.

BRODSCHNEIDER, Robert; CRAILSHEIM, Karl. Nutrition and health in honey bees. Apidologie, vol. 41, no. 3, p. 278–294, 21 May 2010.

CAIRES, Stephanie Castro; BARCELOS, Denise. Colapso das abelhas: Possíveis causas e consequências do seu desaparecimento na natureza. ACTA Apicola Brasilica, vol. 5, no. 1, p. 11–15, 1 Jun. 2017.

CELLI GIROGIO; MACCAGNANI BETTINA. Honey bees as bioindicators of environmental pollution. Bulletin of Insectology, vol. 59(1), p. 137–139, 2003. .

CHANVATIK, Sunicha; DONNUA, Siriporn; LEKAGUL, Angkana; KAEWKHANKHAENG, Wanwisa; VONGMONGKOL, Vuthiphan; ATHIPUNYAKOM, Pornpimon; KHAMLAR, Saenchai; PROMMINTARA, Maitree; TANGCHAROENSATHIEN, Viroj. Antibiotic use in mandarin production (Citrus reticulata Blanco) in major mandarin-producing areas in Thailand: A survey assessment. PLOS ONE, vol. 14, no. 11, p. e0225172, 13 Nov. 2019.

CHEE-SANFORD, Joanne C.; MACKIE, Roderick I.; KOIKE, Satoshi; KRAPAC, Ivan G.; LIN, Yu-Feng; YANNARELL, Anthony C.; MAXWELL, Scott; AMINOV, Rustam I. Fate and Transport of Antibiotic Residues and Antibiotic Resistance Genes following Land Application of Manure Waste. Journal of Environmental Quality, vol. 38, no. 3, p. 1086–1108, May 2009.

CORBET, Sarah A; WILLIAMS, Ingrid H; OSBORNE, Juliet L. Bees and the Pollination of Crops and Wild Flowers in the European Community. Bee World, vol. 72, no. 2, p. 47–59, Jan. 1991.

DANISH TOOR, M.,; ADNAN, M.,; JAVED, M. S.,; HABIBAH, U. E.,; ARSHAD, A.; MUGHEES, M.,; AHMAD, R.,; DANISH, M. Foliar application of Zn: Best way to mitigate drought stress in plants; A review. International Journal of Applied Research, vol. 6(8), p. 16–20, 2020. Available at: Accessed on: 10 Aug. 2023.

DECOURTYE, Axel; DEVILLERS, James. Ecotoxicity of Neonicotinoid Insecticides to Bees. [S. l.: s. n.], 2010. p. 85–95.

DEGRANDI-HOFFMAN, Gloria; ECKHOLM, Bruce J.; HUANG, Ming Hua. A comparison of bee bread made by Africanized and European honey bees (Apis mellifera) and its effects on hemolymph protein titers. Apidologie, vol. 44, no. 1, p. 52–63, 18 Jan. 2013.

DEVEZA, Michele Valadares; KELLER, Kelly Moura; LORENZON, Maria Cristina Affonso; NUNES, Lucila Maria Teixeira; SALES, Érika Oliveira; BARTH, Ortrud Monika. Mycotoxicological and palynological profiles of commercial brands of dried bee pollen. Brazilian Journal of Microbiology, vol. 46, no. 4, p. 1171–1176, Dec. 2015.

DOSCH, Christopher; MANIGK, Anja; STREICHER, Tabea; TEHEL, Anja; PAXTON, Robert J.; TRAGUST, Simon. The Gut Microbiota Can Provide Viral Tolerance in the Honey Bee. Microorganisms, vol. 9, no. 4, p. 871, 17 Apr. 2021.

DYER, Adrian G.; BOYD-GERNY, Skye; MCLOUGHLIN, Stephen; ROSA, Marcello G. P.; SIMONOV, Vera; WONG, Bob B. M. Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision. Proceedings of the Royal Society B: Biological Sciences, vol. 279, no. 1742, p. 3606–3615, 7 Sep. 2012.

ENGEL, Philipp; KWONG, Waldan K.; MCFREDERICK, Quinn; ANDERSON, Kirk E.; BARRIBEAU, Seth Michael; CHANDLER, James Angus; CORNMAN, R. Scott; DAINAT, Jacques; DE MIRANDA, Joachim R.; DOUBLET, Vincent; EMERY, Olivier; EVANS, Jay D.; FARINELLI, Laurent; FLENNIKEN, Michelle L.; GRANBERG, Fredrik; GRASIS, Juris A.; GAUTHIER, Laurent; HAYER, Juliette; KOCH, Hauke; … DAINAT, Benjamin. The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions. mBio, vol. 7, no. 2, 4 May 2016.

ENGEL, Philipp; MARTINSON, Vincent G.; MORAN, Nancy A. Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences, vol. 109, no. 27, p. 11002–11007, 3 Jul. 2012.

ENGEL, Philipp; MORAN, Nancy A. Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut Microbes, vol. 4, no. 1, p. 60–65, 27 Jan. 2013.

FARIA, Ana Carolina Silva de; GODOY, Isabela de; SANCHES, Anderson Aparecido Amorim; IGLESIAS, Gabriela Accardi; CANDIDO, Stefhano Luiz; PAZ, Regina Célia Rodrigues da; NAKAZATO, Luciano; DUTRA, Valéria. Detection of resistance genes and evaluation of water quality at zoo lakes in Brazil. Ciência Rural, vol. 46, no. 5, p. 860–866, May 2016.

FARRER, Emily C.; VAN BAEL, Sunshine A.; CLAY, Keith; SMITH, McKenzie K. H. Plant-Microbial Symbioses in Coastal Systems: Their Ecological Importance and Role in Coastal Restoration. Estuaries and Coasts, vol. 45, no. 7, p. 1805–1822, 30 Nov. 2022.

FORSGREN, Eva; OLOFSSON, Tobias C.; VÁSQUEZ, Alejandra; FRIES, Ingemar. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie, vol. 41, no. 1, p. 99–108, 16 Jan. 2010.

GIANNINI, T. C.; BOFF, S.; CORDEIRO, G. D.; CARTOLANO, E. A.; VEIGA, A. K.; IMPERATRIZ-FONSECA, V. L.; SARAIVA, A. M. Crop pollinators in Brazil: a review of reported interactions. Apidologie, vol. 46, no. 2, p. 209–223, 18 Mar. 2015.

GILL, Richard J.; BALDOCK, Katherine C.R.; BROWN, Mark J.F.; CRESSWELL, James E.; DICKS, Lynn V.; FOUNTAIN, Michelle T.; GARRATT, Michael P.D.; GOUGH, Leonie A.; HEARD, Matt S.; HOLLAND, John M.; OLLERTON, Jeff; STONE, Graham N.; TANG, Cuong Q.; VANBERGEN, Adam J.; VOGLER, Alfried P.; WOODWARD, Guy; ARCE, Andres N.; BOATMAN, Nigel D.; BRAND-HARDY, Richard; … POTTS, Simon G. Protecting an Ecosystem Service. [S. l.: s. n.], 2016. p. 135–206.

GUSSONI, Wilson José; RIBEIRO, Generosa Sousa. Abelhas X Agrotóxicos. Informativo aos apicultores e meliponicultores, , p. 1–16, 2017. .

HAYDAK, M. H. Honey bee nutrition. Annual Review of Entomology, vol. 15(1), p. 143–156, 1970. .

HELANDER, Marjo; JEEVANNAVAR, Aditya; KAAKINEN, Kimmo; MATHEW, Suni A; SAIKKONEN, Kari; FUCHS, Benjamin; PUIGBÒ, Pere; LOUKOLA, Olli J; TAMMINEN, Manu. Glyphosate and a glyphosate-based herbicide affect bumblebee gut microbiota. FEMS Microbiology Ecology, vol. 99, no. 7, 16 Jun. 2023.

HENDRIKSEN, Rene S.; MUNK, Patrick; NJAGE, Patrick; VAN BUNNIK, Bram; MCNALLY, Luke; LUKJANCENKO, Oksana; RÖDER, Timo; NIEUWENHUIJSE, David; PEDERSEN, Susanne Karlsmose; KJELDGAARD, Jette; KAAS, Rolf S.; CLAUSEN, Philip Thomas Lanken Conradsen; VOGT, Josef Korbinian; LEEKITCHAROENPHON, Pimlapas; VAN DE SCHANS, Milou G. M.; ZUIDEMA, Tina; DE RODA HUSMAN, Ana Maria; RASMUSSEN, Simon; PETERSEN, Bent; … AARESTRUP, Frank M. Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. Nature Communications, vol. 10, no. 1, p. 1124, 8 Mar. 2019.


HOPKINS, D. L. Effect of tetracycline antibjotics on pierce ’ s disease of grapevine in florida. Florida State Horticultural Society, vol. 92, p. 284–285, 1979. .

HRISTOV, Peter; NEOV, Boyko; SHUMKOVA, Rositsa; PALOVA, Nadezhda. Significance of Apoidea as Main Pollinators. Ecological and Economic Impact and Implications for Human Nutrition. Diversity, vol. 12, no. 7, p. 280, 15 Jul. 2020.

HUMAN, Hannelie; NICOLSON, Sue W. Nutritional content of fresh, bee-collected and stored pollen of Aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry, vol. 67, no. 14, p. 1486–1492, Jul. 2006.

IWASA, Takao; MOTOYAMA, Naoki; AMBROSE, John T.; ROE, R.Michael. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection, vol. 23, no. 5, p. 371–378, May 2004.

JOHNSON, Renée. Honey bee colony collapse disorder. [S. l.]: Washington: Congressional Research Service, 2010.

JONES, Ben; SHIPLEY, Emily; ARNOLD, Kathryn E. Social immunity in honeybees-Density dependence, diet, and body mass trade-offs. Ecology and Evolution, vol. 8, no. 10, p. 4852–4859, May 2018.

KAČÁNIOVÁ, Miroslava; GASPER, Jaroslav; BRINDZA, Jan; SCHUBERTOVÁ, Zuzana; IVANIŠOVÁ, Eva. Bacteria Of Apis Mellifera Gastrointestinal Tract: Counts, Identification And Their Antibiotic Resistance. [S. l.: s. n.], 2017. p. 210–215.

KERR, Warwick Estevam; ZILSE, Gislene Almeida Carvalho; NASCIMENTO, Vania Alves. Abelha uruçu: biologia, manejo e conservação. Littera Maciel ltda. [S. l.: s. n.], 1996. vol. 2, . Available at: Accessed on: 10 Aug. 2023.

KEŠNEROVÁ, Lucie; MORITZ, Roxane; ENGEL, Philipp. Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. International Journal of Systematic and Evolutionary Microbiology, vol. 66, no. 1, p. 414–421, 1 Jan. 2016.

KHAN, Stuart J.; ONGERTH, Jerry E. Modelling of pharmaceutical residues in Australian sewage by quantities of use and fugacity calculations. Chemosphere, vol. 54, no. 3, p. 355–367, Jan. 2004.

KIELISZEK, Marek; PIWOWAREK, Kamil; KOT, Anna M.; BŁAŻEJAK, Stanisław; CHLEBOWSKA-ŚMIGIEL, Anna; WOLSKA, Iwona. Pollen and bee bread as new health-oriented products: A review. Trends in Food Science & Technology, vol. 71, p. 170–180, Jan. 2018.

KOCH, Hauke; SCHMID-HEMPEL, Paul. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences, vol. 108, no. 48, p. 19288–19292, 29 Nov. 2011.

KWONG, Waldan K.; MANCENIDO, Amanda L.; MORAN, Nancy A. Immune system stimulation by the native gut microbiota of honey bees. Royal Society Open Science, vol. 4, no. 2, p. 170003, Feb. 2017.

LARSEN, Alejandra; REYNALDI, Francisco José; GUZMÁN-NOVOA, Ernesto. Bases del sistema inmune de la abeja melífera (Apis mellifera). Revisión. Revista Mexicana de Ciencias Pecuarias, vol. 10, no. 3, p. 705–728, 11 Sep. 2019.

LAU, Pierre W.; NIEH, James C. Salt preferences of honey bee water foragers. Journal of Experimental Biology, 1 Jan. 2016.

LEE, Fredrick J.; RUSCH, Douglas B.; STEWART, Frank J.; MATTILA, Heather R.; NEWTON, Irene L. G. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environmental Microbiology, vol. 17, no. 3, p. 796–815, Mar. 2015.

LIMA, Valdeir Pereira; MARCHIORO, Cesar Augusto. Brazilian stingless bees are threatened by habitat conversion and climate change. Regional Environmental Change, vol. 21, no. 1, p. 14, 26 Mar. 2021.

LIU, Yueyue; WANG, Chen; QI, Suzhen; WU, Fengchang. Gut Microbiota Provides a New Mechanism for Explaining Agrochemical-Induced Synergistic Effects on Bee Mortality. Environmental Science & Technology, vol. 56, no. 3, p. 1489–1491, 1 Feb. 2022.

MARK E SUÁREZ; BARBARA L THORNE. Rate, amount, and distribution pattern of alimentary fluid transfer via trophallaxis in three species of termites (Isoptera: Rhinotermitidae, Termopsidae). Annals of the Entomological Society of America, vol. 93, no. 1, p. 145–155, 2000. .

MCFALL-NGAI, Margaret; HADFIELD, Michael G.; BOSCH, Thomas C. G.; CAREY, Hannah V.; DOMAZET-LOŠO, Tomislav; DOUGLAS, Angela E.; DUBILIER, Nicole; EBERL, Gerard; FUKAMI, Tadashi; GILBERT, Scott F.; HENTSCHEL, Ute; KING, Nicole; KJELLEBERG, Staffan; KNOLL, Andrew H.; KREMER, Natacha; MAZMANIAN, Sarkis K.; METCALF, Jessica L.; NEALSON, Kenneth; PIERCE, Naomi E.; … WERNEGREEN, Jennifer J. Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences, vol. 110, no. 9, p. 3229–3236, 26 Feb. 2013.

MEYER, M.T; BUMGARNER, J.E; VARNS, Jerry L; DAUGHTRIDGE, J.V; THURMAN, E.M; HOSTETLER, Kenneth A. Use of radioimmunoassay as a screen for antibiotics in confined animal feeding operations and confirmation by liquid chromatography/mass spectrometry. Science of The Total Environment, vol. 248, no. 2–3, p. 181–187, Apr. 2000.

MOHARRAMI, M; MOJGANI, N; BAGHERI, M; TOUTIAEE, S. Role of Honey Bee Gut Microbiota in the Control of American Foulbrood and European Foulbrood Diseases. Archives of Razi Institute, vol. 77, no. 4, p. 1331–1339, Aug. 2022.

MORRIS, Sherri J.; BLACKWOOD, Christopher B. The Ecology of the Soil Biota and their Function. Soil Microbiology, Ecology and Biochemistry. [S. l.]: Elsevier, 2015. p. 273–309.

MOTTA, Erick V. S.; MORAN, Nancy A. Impact of Glyphosate on the Honey Bee Gut Microbiota: Effects of Intensity, Duration, and Timing of Exposure. mSystems, vol. 5, no. 4, 25 Aug. 2020.

MOTTA, Erick V. S.; POWELL, J. Elijah; MORAN, Nancy A. Glyphosate induces immune dysregulation in honey bees. Animal Microbiome, vol. 4, no. 1, p. 16, 22 Dec. 2022.

MOTTA, Erick V. S.; RAYMANN, Kasie; MORAN, Nancy A. Glyphosate perturbs the gut microbiota of honey bees. Proceedings of the National Academy of Sciences, vol. 115, no. 41, p. 10305–10310, 9 Oct. 2018.

MURRAY, Elizabeth A.; BOSSERT, Silas; DANFORTH, Bryan N. Pollinivory and the diversification dynamics of bees. Biology Letters, vol. 14, no. 11, p. 20180530, 28 Nov. 2018.

MUS, Florence; ALLEMAN, Alexander B.; PENCE, Natasha; SEEFELDT, Lance C.; PETERS, John W. Exploring the alternatives of biological nitrogen fixation. Metallomics, vol. 10, no. 4, p. 523–538, 2018.

NARANJO, Eber; MERFA, Marcus V.; SANTRA, Swadeshmukul; OZCAN, Ali; JOHNSON, Evan; COBINE, Paul A.; DE LA FUENTE, Leonardo. Zinkicide Is a ZnO-Based Nanoformulation with Bactericidal Activity against Liberibacter crescens in Batch Cultures and in Microfluidic Chambers Simulating Plant Vascular Systems. Applied and Environmental Microbiology, vol. 86, no. 16, 3 Aug. 2020.

NEGASH, A. Gut Microbiota Ecology Role in Animal Nutrition and Health Performance. Journal of Clinical Microbiology and Antimicrobials, vol. 6 (1000001), p. 1–14, 2022.

NICOLSON, Susan W.; HUMAN, Hannelie; PIRK, Christian W. W. Honey bees save energy in honey processing by dehydrating nectar before returning to the nest. Scientific Reports, vol. 12, no. 1, p. 16224, 28 Sep. 2022.

NOGUEIRA-NETO, Paulo. Inbreeding and building up small populations of stingless bees (Hymenoptera, Apidae). Revista Brasileira de Zoologia, vol. 19, no. 4, p. 1181–1214, Dec. 2002.

PATHAK, Girish Chandra; GUPTA, Bhavana; PANDEY, Nalini. Improving reproductive efficiency of chickpea by foliar application of zinc. Brazilian Journal of Plant Physiology, vol. 24, no. 3, p. 173–180, Sep. 2012.

PENA, A.; PAULO, M.; SILVA, L. J. G.; SEIFRTOVÁ, M.; LINO, C. M.; SOLICH, P. Tetracycline antibiotics in hospital and municipal wastewaters: a pilot study in Portugal. Analytical and Bioanalytical Chemistry, vol. 396, no. 8, p. 2929–2936, 6 Apr. 2010.

POWELL, J. Elijah; LEONARD, Sean P.; KWONG, Waldan K.; ENGEL, Philipp; MORAN, Nancy A. Genome-wide screen identifies host colonization determinants in a bacterial gut symbiont. Proceedings of the National Academy of Sciences, vol. 113, no. 48, p. 13887–13892, 29 Nov. 2016.

POWELL, J. Elijah; MARTINSON, Vincent G.; URBAN-MEAD, Katherine; MORAN, Nancy A. Routes of Acquisition of the Gut Microbiota of the Honey Bee Apis mellifera. Applied and Environmental Microbiology, vol. 80, no. 23, p. 7378–7387, Dec. 2014.

QUIGLEY, Tyler P; AMDAM, Gro V; HARWOOD, Gyan H. Honey bees as bioindicators of changing global agricultural landscapes. Current Opinion in Insect Science, vol. 35, p. 132–137, Oct. 2019.

RAM, Hari; SOHU, V. S.; CAKMAK, Ismail; SINGH, Kuldeep; BUTTAR, G. S.; SODHI, G. P. S.; GILL, H. S.; BHAGAT, Indoo; SINGH, Parminder; DHALIWAL, S. S. Agronomic fortification of rice and wheat grains with zinc for nutritional security. Current Science, vol. 109, no. 6, p. 1171, 17 Sep. 2015.

RAVAIANO, Samira Veiga; BARBOSA, Wagner Faria; CAMPOS, Lúcio Antônio; MARTINS, Gustavo Ferreira. Variations in circulating hemocytes are affected by age and caste in the stingless bee Melipona quadrifasciata. The Science of Nature, vol. 105, no. 7–8, p. 48, 19 Aug. 2018.

RAYMANN, Kasie; SHAFFER, Zack; MORAN, Nancy A. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLOS Biology, vol. 15, no. 3, p. e2001861, 14 Mar. 2017.

REGAN, Tim; BARNETT, Mark W.; LAETSCH, Dominik R.; BUSH, Stephen J.; WRAGG, David; BUDGE, Giles E.; HIGHET, Fiona; DAINAT, Benjamin; DE MIRANDA, Joachim R.; WATSON, Mick; BLAXTER, Mark; FREEMAN, Tom C. Characterisation of the British honey bee metagenome. Nature Communications, vol. 9, no. 1, p. 4995, 26 Nov. 2018.

SANGEETHA, V. J.; DUTTA, Sayantani; MOSES, J. A.; ANANDHARAMAKRISHNAN, C. Zinc nutrition and human health: Overview and implications. eFood, vol. 3, no. 5, 4 Oct. 2022.

SEMIDA, Wael M.; ABDELKHALIK, Abdelsattar; MOHAMED, Gamal. F.; ABD EL-MAGEED, Taia A.; ABD EL-MAGEED, Shimaa A.; RADY, Mostafa M.; ALI, Esmat F. Foliar Application of Zinc Oxide Nanoparticles Promotes Drought Stress Tolerance in Eggplant (Solanum melongena L.). Plants, vol. 10, no. 2, p. 421, 23 Feb. 2021.

SMITH, Matthew R.; MUELLER, Nathaniel D.; SPRINGMANN, Marco; SULSER, Timothy B.; GARIBALDI, Lucas A.; GERBER, James; WIEBE, Keith; MYERS, Samuel S. Pollinator Deficits, Food Consumption, and Consequences for Human Health: A Modeling Study. Environmental Health Perspectives, vol. 130, no. 12, Dec. 2022.

SOARES, Kilmer Oliveira; OLIVEIRA, Celso José Bruno de; RODRIGUES, Adriana Evangelista; VASCONCELOS, Priscylla Carvalho; SILVA, Núbia Michelle Vieira da; CUNHA FILHO, Octavio Gomes da; MADDEN, Christopher; HALE, Vanessa L. Tetracycline Exposure Alters Key Gut Microbiota in Africanized Honey Bees (Apis mellifera scutellata x spp.). Frontiers in Ecology and Evolution, vol. 9, 29 Sep. 2021.

STAVERT, Jamie R.; BAILEY, Charlie; KIRKLAND, Lindsey; RADER, Romina. Pollen tube growth from multiple pollinator visits more accurately quantifies pollinator performance and plant reproduction. Scientific Reports, vol. 10, no. 1, p. 16958, 12 Oct. 2020.

TAN, K.; GUO, Y. H.; NICOLSON, S. W.; RADLOFF, S. E.; SONG, Q. S.; HEPBURN, H. R. Honeybee (Apis cerana) Foraging Responses to the Toxic Honey of Tripterygium hypoglaucum (Celastraceae): Changing Threshold of Nectar Acceptability. Journal of Chemical Ecology, vol. 33, no. 12, p. 2209–2217, 5 Dec. 2007.

TEMPLE, Stanley A. Plant-Animal Mutualism: Coevolution with Dodo Leads to Near Extinction of Plant. Science, vol. 197, no. 4306, p. 885–886, 26 Aug. 1977.

VÁSQUEZ, Alejandra; OLOFSSON, Tobias C. The lactic acid bacteria involved in the production of bee pollen and bee bread. Journal of Apicultural Research, vol. 48, no. 3, p. 189–195, 2 Jan. 2009.

VERNIER, Cassondra L.; CHIN, Iris M.; ADU-OPPONG, Boahemaa; KRUPP, Joshua J.; LEVINE, Joel; DANTAS, Gautam; BEN-SHAHAR, Yehuda. The gut microbiome defines social group membership in honey bee colonies. Science Advances, vol. 6, no. 42, 16 Oct. 2020.

VITOUSEK, Peter M.; MOONEY, Harold A.; LUBCHENCO, Jane; MELILLO, Jerry M. Human Domination of Earth’s Ecosystems. Renewable Energy. [S. l.]: Routledge, 2018. p. 153–166.

WANG, Feng-Hua; QIAO, Min; LV, Zhen-E; GUO, Guang-Xia; JIA, Yan; SU, Yu-Hong; ZHU, Yong-Guan. Impact of reclaimed water irrigation on antibiotic resistance in public parks, Beijing, China. Environmental Pollution, vol. 184, p. 247–253, Jan. 2014.

WANG, Jianwei; MAO, Hui; ZHAO, Hubing; HUANG, Donglin; WANG, Zhaohui. Different increases in maize and wheat grain zinc concentrations caused by soil and foliar applications of zinc in Loess Plateau, China. Field Crops Research, vol. 135, p. 89–96, Aug. 2012.

WARNECKE, Falk; LUGINBÜHL, Peter; IVANOVA, Natalia; GHASSEMIAN, Majid; RICHARDSON, Toby H.; STEGE, Justin T.; CAYOUETTE, Michelle; MCHARDY, Alice C.; DJORDJEVIC, Gordana; ABOUSHADI, Nahla; SOREK, Rotem; TRINGE, Susannah G.; PODAR, Mircea; MARTIN, Hector Garcia; KUNIN, Victor; DALEVI, Daniel; MADEJSKA, Julita; KIRTON, Edward; PLATT, Darren; … LEADBETTER, Jared R. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature, vol. 450, no. 7169, p. 560–565, Nov. 2007.

WASAYA, Allah; SHAHZAD SHABIR, Muhammad; HUSSAIN, Mubshar; ANSAR, Muhammad; AZIZ, Ahsan; HASSAN, Waseem; AHMAD, Ijaz. Foliar application of Zinc and Boron improved the productivity and net returns of maize grown under rainfed conditions of Pothwar plateau. Journal of soil science and plant nutrition, no. ahead, p. 0–0, 2017.

WATKINSON, A.J.; MURBY, E.J.; KOLPIN, D.W.; COSTANZO, S.D. The occurrence of antibiotics in an urban watershed: From wastewater to drinking water. Science of The Total Environment, vol. 407, no. 8, p. 2711–2723, Apr. 2009.

WU, Cindy H.; BERNARD, Stéphanie M.; ANDERSEN, Gary L.; CHEN, Wilfred. Developing microbe-plant interactions for applications in plant-growth promotion and disease control, production of useful compounds, remediation and carbon sequestration. Microbial Biotechnology, vol. 2, no. 4, p. 428–440, Jul. 2009.




How to Cite

Soares, K. O., Hale, V. L., de Medeiros, G. R., da Silva, N. M. V., Lima, M. V., da Rocha, T. F., Maracajá, P. B., Costa, J. H. S., Rodrigues, A. E., & de Oliveira, C. J. B. (2023). The honey bee gut microbiota: a review under the perspective of bees threatened by agrochemicals. OBSERVATÓRIO DE LA ECONOMÍA LATINOAMERICANA, 21(12), 27315–27336.




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