Nutritive and immunological benefits derived from the honey bee gut microbiome are threatened by anthropogenic stressors

Authors

DOI:

https://doi.org/10.17159/2254-8854/2023/a14674

Keywords:

Antibiotics, Bee health, Microbiome, Pesticides, Probiotics

Abstract

Insect gut microbes have a disproportionate effect on their hosts, including the honey bee, Apis mellifera L. The honey bee gut, and that of other species that have been investigated, harbours a specific gut community that is conserved across populations globally. However, this gut community changes between different castes, sexes and life stages, which is largely due to diet and gut physiology. Evidence suggests that a healthy gut community is essential for honey bees to maintain functional immunity and nutrition. Without the four important gut symbionts (Lactobacillus, Bifidobacterium, Snodgrassella alvi and Gilliamella apicola), honey bees lack the ability to gain sufficient nutrients, protect themselves against pathogens and prevent intoxication. Unfortunately, honey bee gut symbionts are under threat due to in-hive pesticides, antibiotics and climate change. Therefore, we discourage the overuse of antibiotics and in-hive pesticides, as they could have unforeseen consequences for the honey bee gut microbiota. Instead, we recommend that beekeepers and scientists explore alternative options, such as bolstering honey bee resilience through probiotics.

Downloads

Download data is not yet available.

References

Abudulai M, Nboyine JA, Quandahor P, Seidu A, Traore F. 2022. Agricultural intensification causes decline in insect biodiversity. In: Hamadttu Abdel Farag El-Shafie, editor. Global Decline of Insects. London: IntechOpen. https://doi.org/ 10.5772/intechopen.101360.

Al Naggar Y, Singavarapu B, Paxton RJ, Wubet T. 2022. 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 849:157941. https://doi.org/10.1016/j.scitotenv.2022.157941

Almasri H, Liberti J, Brunet J-L, Engel P, Belzunces LP. 2022. Mild chronic exposure to pesticides alters physiological markers of honey bee health without perturbing the core gut microbiota. Scientific Reports 12(1):4281. https://doi.org/10.1038/s41598-022-08009-2.

Amato KR. 2013. Co-evolution in context: the importance of studying gut microbiomes in wild animals. Microbiome Science and Medicine 1: 10–29. https://doi.org/ 10.2478/micsm-2013-0002

Anderson KE, Ricigliano, VA, Copeland DC. Mott BM, Maes P. 2023. Social interaction is unnecessary for hindgut microbiome transmission in honey bees: The effect of diet and social exposure on tissue-specific microbiome assembly. Microbial Ecology 85(4):1498–1513. https://doi.org/10.1007/s00248-022-02025-5

Aufauvre J, Misme-Aucouturier B, Viguès B, Texier C, Delbac F, Blot N. 2014. Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLoS One 9(3):e91686. https://doi.org/10.1371/journal.pone.0091686

Boncristiani H, Ellis JD, Bustamante T, Graham J, Jack C, Kimmel CB, Mortensen A, Schmehl DR. 2021. World honey bee health: the global distribution of western honey bee (Apis mellifera L.) pests and pathogens. Bee World. 98(1):2–6. https://doi.org/10.1080/0005772X.2020.1800330

Bonilla-Rosso G, Engel P. 2018, Functional roles and metabolic niches in the honey bee gut microbiota. Current Opinion in Microbiology 43:69–76. https://doi.org/10.1016/j.mib.2017.12.009

Bonilla-Rosso G, Steiner T, Wichmann F, Bexkens E, Engel P. 2020. Honey bees harbor a diverse gut virome engaging in nested strain-level interactions with the microbiota. Proceedings of the National Academy of Sciences 117(13):7355–7362. https://doi.org/10.1073/pnas.2000228117

Brochet S, Quinn A, Mars RA, Neuschwander N, Sauer U, Engel P. 2021. Niche partitioning facilitates coexistence of closely related honey bee gut bacteria. eLife. 10:e68583. https://doi.org/10.7554/eLife.68583

Burritt NL, Foss NJ, Neeno-Eckwall EC, Church JO, Hilger AM, Hildebrand JA, Warshauer DM, Perna NT, Burritt JB. Sepsis and hemocyte loss in honey bees (Apis mellifera) infected with Serratia marcescens strain sicaria. PLoS One 11(12):e0167752. https://doi.org/10.1371/journal.pone.0167752

Cardoso P, Leather SR. 2019. Predicting a global insect apocalypse. Insect Conservation and Diversity 12:263–267. https://doi.org/10.1111/icad.12367

Cariveau DP, Elijah Powell J, Koch H, Winfree R, Moran NA. 2014.Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). The ISME Journal 8(12):2369–2379. https://doi.org/10.1038/ismej.2014.68

Cobián Güemes AG, Youle M, Cantú VA, Felts B, Nulton J, Rohwer F. 2016. Viruses as winners in the game of life. Annual Review of Virology 3(1):197–214. https://doi.org/10.1146/annurev-virology-100114-054952

Contrera F, Imperatriz-Fonseca V, Koedam D. 2010. Trophallaxis and reproductive conflicts in social bees. Insectes Sociaux 57(2):125–132. https://doi.org/10.1007/s00040-009-0058-5

Corby-Harris V, Maes P, Anderson KE. 2014. The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS One 9(4):e95056. https://doi.org/10.1371/journal.pone.0095056

Crotti E, Sansonno L, Prosdocimi EM, Vacchini V, Hamdi C, Cherif A, Gonella E, Marzorati M, Balloi A. 2013. Microbial symbionts of honeybees: a promising tool to improve honeybee health. New Biotechnology 30(6):716–722. https://doi.org/10.1016/j.nbt.2013.05.004

Cunningham MM, Tran L, McKee CG, Ortega Polo R, Newman T, Lansing L, Griffiths JS, Bilodeau GJ, Rott M, Marta Guarna M. 2022. Honey bees as biomonitors of environmental contaminants, pathogens, and climate change. Ecological Indicators 134:108457. https://doi.org/10.1016/j.ecolind.2021.108457

Daisley BA, Pitek AP, Chmiel JA, Gibbons S, Chernyshova AM, Al KF, Faragalla KM, Burton JP, Thompson GJ, Reid G. 2020. Lactobacillus spp. attenuate antibiotic-induced immune and microbiota dysregulation in honey bees. Communications Biology 3(1):534. https://doi.org/10.1038/s42003-020-01259-8

Dietemann V, Pirk CWW, Crewe R. 2009. Is there a need for conservation of honeybees in Africa? Apidologie (Celle) 40(3):285–295. https://doi.org/10.1051/apido/2009013

Dosch C, Manigk A, Streicher T, Tehel A, Paxton RJ, Tragust S. 2021. The gut microbiota can provide viral tolerance in the honey bee. Microorganisms 9(4):871. https://doi.org/10.3390/microorganisms9040871

Du Rand EE, Stutzer C, Human H, Pirk CWW, Nicolson SW. 2020. Antibiotic treatment impairs protein digestion in the honeybee, Apis mellifera. Apidologie (Celle) 51(1):94–106. https://doi.org/10.1007/s13592-019-00718-4

Ellis J. 2012. The honey bee crisis. Outlooks Pest Management 23(1):35–40. https://doi.org/10.1564/22feb10

Elzeini HM, Ali ARAA, Nasr NF, Hassan M, Hassan AA, Elenany YE. 2021. Probiotic capability of novel lactic acid bacteria isolated from worker honey bees gut microbiota. FEMS Microbiology Letters 368(6):fnab030. https://doi.org/10.1093/femsle/fnab030

Emery O, Schmidt K, Engel P. 2017. Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera). Molecular Ecology 26(9):2576–2590. https://doi.org/10.1111/mec.14058

Engel P, Martinson VG, Moran NA. 2012. Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences 109(27):11002–11007. https://doi.org/10.1073/pnas.1202970109

Engel P, Moran NA. 2013. The gut microbiota of insects–diversity in structure and function. FEMS Microbiology Reviews 37(5):699–735. https://doi.org/10.1111/1574-6976.12025

Engel P, Bartlett KD, Moran NA. 2015. The bacterium Frischella perrara causes scab formation in the gut of its honeybee host. mBio 6(3):e00193-15. https://doi.org/10.1128/mBio.00193-15

Evans JD. 2003. Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae. Journal of Invertebrate Pathology 83(1):46–50. https://doi.org/10.1016/S0022-2011(03)00039-9

Fahrenholz L, Lamprecht I, Schricker B. 1989. Thermal investigations of a honey bee colony: thermoregulation of the hive during summer and winter and heat production of members of different bee castes. Journal of Comparative Physiology B 159(5):551–560. https://doi.org/10.1007/BF00694379

Forsgren E, Olofsson TC, Vásquez A, Fries I. 2010. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie (Celle) 41(1):99–108. https://doi.org/10.1051/apido/2009065

Gallai N, Salles J-M, Settele J, Vaissière BE. 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68(3):810–821. https://doi.org/10.1016/j.ecolecon.2008.06.014

Genersch E. 2010. Honey bee pathology: current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology 87(1):87–97. https://doi.org/10.1007/s00253-010-2573-8

Goulson D, Nicholls E, Botías C, Rotheray EL. 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229):1255957. https://doi.org/10.1126/science.1255957

Guo J, Wu J, Chen Y, Evans JD, Dai R, Luo W, Li J. 2015. Characterization of gut bacteria at different developmental stages of Asian honey bees, Apis cerana. Journal of Invertebrate Pathology 127:110–114. https://doi.org/10.1016/j.jip.2015.03.010

Habineza P, Muhammad A, Ji T, Xiao R, Yin X, Hou Y, Shi Z. 2019. The promoting effect of gut microbiota on growth and development of red palm weevil, Rhynchophorus ferrugineus (Olivier)(Coleoptera: Dryophthoridae) by modulating its nutritional metabolism. Frontiers in Microbiology 10:1212. https://doi.org/10.3389/fmicb.2019.01212.

Hacquard S, Garrido-Oter R, González A, Spaepen S, Ackermann G, Lebeis S, McHardy AC, Dangl JL, Knight R, Ley R, et al. 2015. Microbiota and host nutrition across plant and animal kingdoms. Cell Host & Microbe 17(5):603–616. https://doi.org/10.1016/j.chom.2015.04.009

Halvorson K, Baumung R, Leroy G, Chen C, Boettcher P. 2021. Protection of honeybees and other pollinators: one global study. Apidologie (Celle) 52(3):535–547. https://doi.org/10.1007/s13592-021-00841-1

Harvey JA, Tougeron K, Gols R, Heinen R, Abarca M, Abram PK, Basset Y, Berg M, Boggs C, Brodeur J, et al. 2023. Scientists’ warning on climate change and insects. Ecological Monographs 93(1):e1553. https://doi.org/10.1002/ecm.1553

Human H, Nicolson SW, Strauss K, Pirk CWW, Dietemann V. 2007. Influence of pollen quality on ovarian development in honeybee workers (Apis mellifera scutellata). Journal of Insect Physiology 53(7):649–655. https://doi.org/10.1016/j.jinsphys.2007.04.002

Human H, Pirk CWW, Crewe RM, Dietemann V. 2011. The honeybee disease American foulbrood—an African perspective. African Entomology 19(2):551–557. https://doi.org/10.4001/003.019.0301

Hung K-LJ, Kingston JM, Albrecht M, Holway DA, Kohn JR. 2018. The worldwide importance of honey bees as pollinators in natural habitats. Proceedings of the Royal Society B: Biological Sciences 285(1870):20172140. https://doi.org/10.1098/rspb.2017.2140

Kakumanu ML, Reeves AM, Anderson TD, Rodrigues RR, Williams MA. 2016. Honey bee gut microbiome is altered by in-hive pesticide exposures. Frontiers in Microbiology 7:1255. https://doi.org/10.3389/fmicb.2016.01255

Kapheim KM, Rao VD, Yeoman CJ, Wilson BA, White BA, Goldenfeld N, Robinson GE. 2015. Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PLoS One 10(4):e0123911. https://doi.org/10.1371/journal.pone.0123911

Karl TR, Trenberth KE. 2003. Modern global climate change. Science 302(5651):1719–1723. https://doi.org/10.1126/science.1090228

Kikuchi Y, Hosokawa T, Fukatsu T. 2007. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Applied Environmental Microbiology 73(13):4308–4316. https://doi.org/10.1128/AEM.00067-07

Kikuchi Y, Tada A, Musolin DL, Hari N, Hosokawa T, Fujisaki K, Fukatsu T. 2016. Collapse of insect gut symbiosis under simulated climate change. mBio 7(5):e01578-16. https://doi.org/10.1128/mbio.01578-16

Koch, H. & Schmid-Hempel, P. 2011. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences 108:19288–19292. https://doi.org/10.1073/pnas.1110474108

Koch H, Cisarovsky G, Schmid, Hempel P. 2012. Ecological effects on gut bacterial communities in wild bumblebee colonies. Journal of Animal Ecology 81(6):1202–1210. https://doi.org/10.1111/j.1365-2656.2012.02004.x

Kowallik V, Mikheyev AS. 2021. Honey bee larval and adult microbiome life stages are effectively decoupled with vertical transmission overcoming early life perturbations. MBio 12(6):e02966–21. https://doi.org/10.1128/mBio.02966-21

Kuziel GA, Rakoff-Nahoum S. 2022. The gut microbiome. Current Biology 32(6):R257–R264. https://doi.org/10.1016/j.cub.2022.02.023.

Kwong WK, Moran NA. 2013. Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology 63(Pt_6):2008–2018. https://doi.org/10.1099/ijs.0.044875-0.

Kwong WK, Engel P, Koch H, Moran NA. 2014. Genomics and host specialization of honey bee and bumble bee gut symbionts. Proceedings of the National Academy of Sciences 111(31):11509–11514. https://doi.org/10.1073/pnas.1405838111

Kwong WK, Moran NA. 2016. Gut microbial communities of social bees. Nature Reviews Microbiology 14(6):374–384. https://doi.org/10.1038/nrmicro.2016.43

Kwong WK, Mancenido AL, Moran NA. 2017. Immune system stimulation by the native gut microbiota of honey bees. Royal Society Open Science 4(2):170003. https://doi.org/10.1098/rsos.170003

Labandeira CC, Sepkoski JJ Jr. 1993. Insect diversity in the fossil record. Science 261(5119):310–315. https://doi.org/10.1126/science.11536548

Lang H, Duan H, Wang J, Zhang W, Guo J, Zhang X, Hu X, Zheng H. 2022. Specific strains of honeybee gut Lactobacillus stimulate host immune system to protect against pathogenic Hafnia alvei. Microbiology Spectrum 10(1):e01896–21. https://doi.org/10.1128/spectrum.01896-21

Langridge D, McGhee RB. 1967. Crithidia mellificae n. sp. an acidophilic trypanosomatid of the honey bee Apis mellifera. The Journal of Protozoology 14(3):485–487. https://doi.org/10.1111/j.1550-7408.1967.tb02033.x

Lee FJ, Rusch DB, Stewart FJ, Mattila HR, Newton IL. 2015. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environmental Microbiology 17(3):796–815. https://doi.org/10.1111/1462-2920.12526

Lee FJ, Miller KI, McKinlay JB, Newton IL. 2018. Differential carbohydrate utilization and organic acid production by honey bee symbionts. FEMS Microbiology Ecology 94(8):fiy113. https://doi.org/10.1093/femsec/fiy113

Lee MJ, Schreurs PJ, Messer AC, Zinder SH. 1987. Association of methanogenic bacteria with flagellated protozoa from a termite hindgut. Current Microbiology 15(6):337–341. https://doi.org/10.1007/BF01577591

Lee W-J, Hase K. 2014. Gut microbiota–generated metabolites in animal health and disease. Nature Chemical Biology 10(6):416–424. https://doi.org/10.1038/nchembio.1535

Leita L, Muhlbachova G, Cesco S, Barbattini R, Mondini C. 1996 Investigation of the use of honey bees and honey bee products to assess heavy metals contamination. Environmental Monitoring and Assessment 43(1):1–9. https://doi.org/10.1007/BF00399566

Li JH, Evans JD, Li WF, Zhao YZ, DeGrandi-Hoffman G, Huang SK, Li ZG, Hamilton M, Chen YP. 2017. New evidence showing that the destruction of gut bacteria by antibiotic treatment could increase the honey bee’s vulnerability to Nosema infection. PLoS One 12(11):e0187505. https://doi.org/10.1371/journal.pone.0187505

Lozo J, Berić T, Terzić-Vidojević A, Stanković S, Fira D, Stanisavljević L. 2015. Microbiota associated with pollen, bee bread, larvae and adults of solitary bee Osmia cornuta (Hymenoptera: Megachilidae). Bulletin of Entomological Research 105(4):470–476. https://doi.org/10.1017/S0007485315000292

Lusebrink I, Girling RD, Farthing E, Newman TA, Jackson CW, Poppy GM. 2015. The effects of diesel exhaust pollution on floral volatiles and the consequences for honey bee olfaction. Journal of Chemical Ecology 41(10):904–912. https://doi.org/10.1007/s10886-015-0624-4

Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA. 2011. A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology 20(3):619–628. https://doi.org/10.1111/j.1365-294X.2010.04959.x

Martinson VG, Moy J, Moran NA. 2012. Establishment of characteristic gut bacteria during development of the honeybee worker. Applied and Environmental Microbiology 78(8):2830–2840. https://doi.org/10.1128/AEM.07810-11

Maruščáková IC, Schusterová P, Bielik B, Toporčák J, Bíliková K, Mudroňová D. 2020. Effect of application of probiotic pollen suspension on immune response and gut microbiota of honey bees (Apis mellifera). Probiotics and Antimicrobial Proteins 12(3):929–936. https://doi.org/10.1007/s12602-019-09626-6

Motta EV, Raymann K, Moran NA. 2018. Glyphosate perturbs the gut microbiota of honey bees. roceedings of the National Academy of Sciences 115(41):10305–10310. https://doi.org/10.1073/pnas.1803880115

Motta EV, Mak M, De Jong TK, Powell JE, O’Donnell A, Suhr KJ, Riddington IM, Moran NA. 2020. Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees. Applied and Environmental Microbiology 86(18):e01150–20. https://doi.org/10.1128/AEM.01150-20

Motta EV, Powell JE, Leonard SP, Moran NA. Prospects for probiotics in social bees. Philosophical Transactions of the Royal Society B 2022;377(1853):20210156. https://doi.org/10.1098/rstb.2021.0156.

Nicolson SW, Da Silva Das Neves S, Human H, Pirk CWW. 2018. Digestibility and nutritional value of fresh and stored pollen for honey bees (Apis mellifera scutellata). Journal of Insect Physiology 107:302–308. https://doi.org/10.1016/j.jinsphys.2017.12.008

Olofsson TC, Vásquez A. 2008. Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Current Microbiology 57(4):356–363. https://doi.org/10.1007/s00284-008-9202-0

Pal S, Karmakar P. 2018. Symbionts associated with insect digestive system and their role in insect nutrition. Journal of Entomology and Zoology Studies 6:421–425.

Parish AJ, Rice DW, Tanquary VM, Tennessen JM, Newton IL. 2022. Honey bee symbiont buffers larvae against nutritional stress and supplements lysine. The ISME Journal 16(9):2160–2168. https://doi.org/10.1038/s41396-022-01268-x

Pirk CWW, Human H, Crewe RM, VanEngelsdorp D. 2014. A survey of managed honey bee colony losses in the Republic of South Africa–2009 to 2011. Journal of Apicultural Research 53(1):35–42. https://doi.org/10.3896/IBRA.1.53.1.03

Pirk CWW, Strauss U, Yusuf AA, Démares F, Human H. 2016. Honeybee health in Africa—a review. Apidologie (Celle) 47(3):276–300. https://doi.org/10.1007/s13592-015-0406-6.

Powell JE, Carver Z, Leonard SP, Moran NA. 2021. Field-realistic tylosin exposure impacts honey bee microbiota and pathogen susceptibility, which is ameliorated by native gut probiotics. Microbiology Spectrum 9(1):e00103–21. https://doi.org/10.1128/Spectrum.00103-21

Prado SS, Hung KY, Daugherty MP, Almeida RP. 2010. Indirect effects of temperature on stink bug fitness, via maintenance of gut-associated symbionts. Applied Environmental Microbiology 76(4):1261–1266. https://doi.org/10.1128/AEM.02034-09.

Praet J, Meeus I, Cnockaert M, Houf K, Smagghe G, Vandamme P. 2015 Novel lactic acid bacteria isolated from the bumble bee gut: Convivina intestini gen. nov., sp. nov., Lactobacillus bombicola sp. nov., and Weissella bombi sp. nov. Antonie van Leeuwenhoek 107(5):1337–1349. https://doi.org/10.1007/s10482-015-0429-z

Ptaszyńska AA, Borsuk G, Zdybicka-Barabas A, Cytryńska M, Małek W. 2016. Are commercial probiotics and prebiotics effective in the treatment and prevention of honeybee nosemosis C? Parasitology Reserch 115(1):397–406. https://doi.org/10.1007/s00436-015-4761-z

Raymann K, Shaffer Z, Moran NA. 2017. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol 15(3): e2001861 https://doi.org/10.1371/journal.pbio.2001861

Raymann K, Moran NA. 2018. The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science 26:97–104. https://doi.org/10.1016/j.cois.2018.02.012

Requier F, Garnery L, Kohl PL, Njovu HK, Pirk CWW, Crewe RM, Steffan-Dewenter I. 2019. The conservation of native honey bees is crucial. Trends in Ecology & Evolution 34(9):789–798. https://doi.org/10.1016/j.tree.2019.04.008

Romero S, Nastasa A, Chapman A, Kwong W, Foster L. 2019. The honey bee gut microbiota: strategies for study and characterization. Insect Molecular Biology 28(4):455–472. https://doi.org/10.1111/imb.12567

Saelao P, Borba RS, Ricigliano V, Spivak M, Simone-Finstrom M. 2020. Honeybee microbiome is stabilized in the presence of propolis. Biology Letters 16(5):20200003. https://doi.org/10.1098/rsbl.2020.0003

Sánchez-Bayo F, Wyckhuys KA. 2019. Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation 232:8–27. https://doi.org/10.1016/j.biocon.2019.01.020

Snodgrass RE. 1910. The thorax of the Hymenoptera. Proceedings of the United States National Museum 39(1774): 37–91.

Steele MI, Motta EVS, Gattu T, Martinez D, Moran NA. 2021. The gut microbiota protects bees from invasion by a bacterial pathogen. Microbiology Spectrum 9(2):e0039421. https://doi.org/10.1128/Spectrum.00394-21

Stein K, Coulibaly D, Stenchly K, Goetze D, Porembski S, Lindner A, Konaté S, Linsenmair EK. 2017. Bee pollination increases yield quantity and quality of cash crops in Burkina Faso, West Africa. Scientific Reports 7(1):17691. https://doi.org/10.1038/s41598-017-17970-2

Steinigeweg C, Alkassab AT, Erler S, Beims H, Wirtz IP, Richter D, Pistorius J. 2023. Impact of a microbial pest control product containing Bacillus thuringiensis on brood development and gut microbiota of Apis mellifera worker honey bees. Microbial Ecology ; 85(4):1300-1307. https://doi.org/10.1007/s00248-022-02004-w

Stork NE. 1988. Insect diversity: facts, fiction and speculation. Biological journal of the Linnean Society 35(4):321–337. https://doi.org/10.1111/j.1095-8312.1988.tb00474.x

Traynor KS, Pettis JS, Tarpy DR, Mullin CA, Frazier JL, Frazier M, van Engelsdorp D. 2016. In-hive pesticide exposome: assessing risks to migratory honey bees from in-hive pesticide contamination in the Eastern United States. Scientific Reports 6(1):33207. https://doi.org/10.1038/srep33207

Vacharaksa A, Finlay B. 2010. Gut microbiota: metagenomics to study complex ecology. Current Biology 20(13):R569–R571. https://doi.org/10.1016/j.cub.2010.05.020.

Vanbergen, A. 2013. The insect pollinators initiative. BBKA News 21-28.

Weisser W, Blüthgen N, Staab M, Achury R, Müller J. 2023. Experiments are needed to quantify the main causes of insect decline. Biological Letters 19(2):20220500. https://doi.org/10.1098/rsbl.2022.0500

Wu Y, Zheng Y, Chen Y, Wang S, Chen Y, Hu F, Zheng H. 2020. Honey bee (Apis mellifera) gut microbiota promotes host endogenous detoxification capability via regulation of P450 gene expression in the digestive tract. Microbial Biotechnology 13(4):1201–1212. https://doi.org/10.1111/1751-7915.13579

Ye M-H, Fan S-H, Li X-Y, Tarequl IM, Yan C-X, Wei W-H, Yang S-M, Zhou B. 2021. Microbiota dysbiosis in honeybee (Apis mellifera L.) larvae infected with brood diseases and foraging bees exposed to agrochemicals. Royal Society Open Science 8:201805. https://doi.org/10.1098/rsos.201805

Yun J-H, Jung M-J, Kim PS, Bae J-W. 2018. Social status shapes the bacterial and fungal gut communities of the honey bee. Scientific Reports 8: 2019 (2018). https://doi.org/10.1038/s41598-018-19860-7

Zheng H, Nishida A, Kwong WK, Koch H, Engel P, Steele MI, Moran NA. 2016. Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola. MBio 7(6):e01326–16. https://doi.org/10.1128/mBio.01326-16

Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA. 2017. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proceedings of the National Academy of Sciences 114(18):4775–4780. https://doi.org/10.1073/pnas.1701819114

Zheng H, Steele MI, Leonard SP, Motta EV, Moran NA. 2018. Honey bees as models for gut microbiota research. Lab Animal (NY) 47(11):317–325. https://doi.org/10.1038/s41684-018-0173-x

Zhu L, Qi S, Xue X, Niu X, Wu L. 2020. Nitenpyram disturbs gut microbiota and influences metabolic homeostasis and immunity in honey bee (Apis mellifera L.). Environmental Pollution 258:113671. https://doi.org/10.1016/j.envpol.2019.113671

Zhukova M, Sapountzis P, Schiøtt M, Boomsma JJ. 2017. Diversity and transmission of gut bacteria in Atta and Acromyrmex leaf-cutting ants during development. Frontiers in Microbiology 8:1942. https://doi.org/10.3389/fmicb.2017.01942

Downloads

Published

2023-08-08

Issue

Section

Articles

How to Cite

1.
Nutritive and immunological benefits derived from the honey bee gut microbiome are threatened by anthropogenic stressors. Afr. Entomol. [Internet]. 2023 Aug. 8 [cited 2024 Nov. 19];31. Available from: https://www.africanentomology.com/article/view/14674