Polyphenols as Food Supplement Improved Food Consumption and Longevity of Honey Bees (Apis mellifera) Intoxicated by Pesticide Thiacloprid
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
AF-IGA2019-IP007
Mendelova Univerzita v Brně
QK1910356
Ministerstvo Zemědělství
PubMed
34201457
PubMed Central
PMC8304825
DOI
10.3390/insects12070572
PII: insects12070572
Knihovny.cz E-zdroje
- Klíčová slova
- cage experiments, cytochrome P450, detoxification, food intake, mortality rate,
- Publikační typ
- časopisecké články MeSH
Malnutrition is one of the main problems related to the global mass collapse of honey bee colonies, because in honey bees, malnutrition is associated with deterioration of the immune system and increased pesticide susceptibility. Another important cause of mass bee colonies losses is the use of pesticides. Therefore, the goal of this study was to verify the influence of polyphenols on longevity, food consumption, and cytochrome P450 gene expression in worker bees intoxicated by thiacloprid. The tests were carried out in vitro under artificial conditions (caged bees). A conclusively lower mortality rate and, in parallel, a higher average food intake, were observed in intoxicated bees treated using a mixture of phenolic acids and flavonoids compared to untreated intoxicated bees. This was probably caused by increased detoxification capacity caused by increased expression level of genes encoding the cytochrome P450 enzyme in the bees. Therefore, the addition of polyphenols into bee nutrition is probably able to positively affect the detoxification capacity of bees, which is often reduced by the impact of malnutrition resulting from degradation of the environment and common beekeeping management.
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Aizen M.A., Garibaldi L.A., Cunningham S.A., Klein A.M. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann. Bot. 2009;103:1579–1588. doi: 10.1093/aob/mcp076. PubMed DOI PMC
Stokstad E. The Case of the Empty Hives. Science. 2007;316:970–972. doi: 10.1126/science.316.5827.970. PubMed DOI
Brodschneider R., Crailsheim K. Nutrition and Health in Honey Bees. Apidologie. 2010;41:278–294. doi: 10.1051/apido/2010012. DOI
Di Pasquale G., Salignon M., Le Conte Y., Belzunces L.P., Decourtye A., Kretzschmar A., Suchail S., Brunet J.-L., Alaux C. Influence of Pollen Nutrition on Honey Bee Health: Do Pollen Quality and Diversity Matter? PLoS ONE. 2013;8:e72016. doi: 10.1371/journal.pone.0072016. PubMed DOI PMC
Sharpe R.J., Heyden L.C. Honey Bee Colony Collapse Disorder Is Possibly Caused by a Dietary Pyrethrum Deficiency. Biosci. Hypotheses. 2009;2:439–440. doi: 10.1016/j.bihy.2009.01.004. DOI
Haydak M.H. Honey Bee Nutrition. Annu. Rev. Entomol. 1970;15:143–156. doi: 10.1146/annurev.en.15.010170.001043. DOI
Naug D. Nutritional Stress Due to Habitat Loss May Explain Recent Honeybee Colony Collapses. Biol. Conserv. 2009;142:2369–2372. doi: 10.1016/j.biocon.2009.04.007. DOI
Johnson R.M., Ellis M.D., Mullin C.A., Frazier M. Pesticides and Honey Bee Toxicity—USA. Apidologie. 2010;41:312–331. doi: 10.1051/apido/2010018. DOI
Decourtye A., Mader E., Desneux N. Landscape Enhancement of Floral Resources for Honey Bees in Agro-Ecosystems. Apidologie. 2010;41:264–277. doi: 10.1051/apido/2010024. DOI
Manning R., Rutkay A., Eaton L., Dell B. Lipid-enhanced Pollen and Lipid-reduced Flour Diets and Their Effect on the Longevity of Honey Bees (Apis mellifera L.) Aust. J. Entomol. 2007;46:251–257. doi: 10.1111/j.1440-6055.2007.00598.x. DOI
Hayes J., Jr., Underwood R.M., Pettis J. A Survey of Honey Bee Colony Losses in the US, Fall 2007 to Spring 2008. PLoS ONE. 2008;3:e4071. PubMed PMC
Wahl O., Ulm K. Influence of Pollen Feeding and Physiological Condition on Pesticide Sensitivity of the Honey Bee Apis mellifera Carnica. Oecologia. 1983;59:106–128. doi: 10.1007/BF00388082. PubMed DOI
Alaux C., Ducloz F., Crauser D., Le Conte Y. Diet Effects on Honeybee Immunocompetence. Biol. Lett. 2010;6:562–565. doi: 10.1098/rsbl.2009.0986. PubMed DOI PMC
Keller I., Fluri P., Imdorf A. Pollen Nutrition and Colony Development in Honey Bees—Part II. Bee World. 2005;86:27–34. doi: 10.1080/0005772X.2005.11099650. DOI
Frazier M., Mullin C., Frazier J., Ashcraft S. What Have Pesticides Got to Do with It? Am. Bee J. 2008;148:521–524.
Medrzycki P., Sgolastra F., Bortolotti L., Bogo G., Tosi S., Padovani E., Porrini C., Sabatini A.G. Influence of Brood Rearing Temperature on Honey Bee Development and Susceptibility to Poisoning by Pesticides. J. Apic. Res. 2010;49:52–59. doi: 10.3896/IBRA.1.49.1.07. DOI
Iwasa T., Motoyama N., Ambrose J.T., Roe R.M. Mechanism for the Differential Toxicity of Neonicotinoid Insecticides in the Honey Bee, Apis mellifera. Crop Prot. 2004;23:371–378. doi: 10.1016/j.cropro.2003.08.018. DOI
Alaux C., Brunet J., Dussaubat C., Mondet F., Tchamitchan S., Cousin M., Brillard J., Baldy A., Belzunces L.P., Le Conte Y. Interactions between Nosema Microspores and a Neonicotinoid Weaken Honeybees (Apis mellifera) Environ. Microbiol. 2010;12:774–782. doi: 10.1111/j.1462-2920.2009.02123.x. PubMed DOI PMC
Retschnig G., Neumann P., Williams G.R. Thiacloprid–Nosema Ceranae Interactions in Honey Bees: Host Survivorship but Not Parasite Reproduction Is Dependent on Pesticide Dose. J. Invertebr. Pathol. 2014;118:18–19. doi: 10.1016/j.jip.2014.02.008. PubMed DOI
Suchail S., Guez D., Belzunces L.P. Characteristics of Imidacloprid Toxicity in Two Apis mellifera Subspecies. Environ. Toxicol. Chem. 2000;19:1901–1905. doi: 10.1002/etc.5620190726. DOI
Nauen R., Ebbinghaus-Kintscher U., Schmuck R. Toxicity and Nicotinic Acetylcholine Receptor Interaction of Imidacloprid and Its Metabolites in Apis mellifera (Hymenoptera: Apidae) Pest Manag. Sci. 2001;57:577–586. doi: 10.1002/ps.331. PubMed DOI
Wehling M., Ohe W., Brasse D., Forster R. Colony Losses-Interactions of Plant Protection Products and Other Factors. Jul. Kühn Arch. 2009;423:153–154.
Grillone G., Laurino D., Manino A., Porporato M. Toxicity of Thiametoxam on in vitro Reared Honey Bee Brood. Apidologie. 2017;48:635–643. doi: 10.1007/s13592-017-0506-6. DOI
Osterman J., Wintermantel D., Locke B., Jonsson O., Semberg E., Onorati P., Forsgren E., Rosenkranz P., Rahbek-Pedersen T., Bommarco R. Clothianidin Seed-Treatment Has No Detectable Negative Impact on Honeybee Colonies and Their Pathogens. Nat. Commun. 2019;10:1–13. doi: 10.1038/s41467-019-08523-4. PubMed DOI PMC
Rundlöf M., Lundin O. Can Costs of Pesticide Exposure for Bumblebees Be Balanced by Benefits from a Mass-Flowering Crop? Environ. Sci. Technol. 2019;53:14144–14151. doi: 10.1021/acs.est.9b02789. PubMed DOI
Ghazoul J. Buzziness as Usual? Questioning the Global Pollination Crisis. Trends Ecol. Evol. 2005;20:367–373. doi: 10.1016/j.tree.2005.04.026. PubMed DOI
Alburaki M., Boutin S., Mercier P.-L., Loublier Y., Chagnon M., Derome N. Neonicotinoid-Coated Zea Mays Seeds Indirectly Affect Honeybee Performance and Pathogen Susceptibility in Field Trials. PLoS ONE. 2015;10:e0125790. doi: 10.1371/journal.pone.0125790. PubMed DOI PMC
Claudianos C., Ranson H., Johnson R., Biswas S., Schuler M., Berenbaum M., Feyereisen R., Oakeshott J.G. A Deficit of Detoxification Enzymes: Pesticide Sensitivity and Environmental Response in the Honeybee. Insect Mol. Biol. 2006;15:615–636. doi: 10.1111/j.1365-2583.2006.00672.x. PubMed DOI PMC
Mao W., Schuler M., Berenbaum M. Task-related Differential Expression of Four Cytochrome P450 Genes in Honeybee Appendages. Insect Mol. Biol. 2015;24:582–588. doi: 10.1111/imb.12183. PubMed DOI
Mao W., Schuler M.A., Berenbaum M.R. Honey Constituents Up-Regulate Detoxification and Immunity Genes in the Western Honey Bee Apis mellifera. Proc. Natl. Acad. Sci. USA. 2013;110:8842–8846. doi: 10.1073/pnas.1303884110. PubMed DOI PMC
Liao L.-H., Wu W.-Y., Berenbaum M.R. Impacts of Dietary Phytochemicals in the Presence and Absence of Pesticides on Longevity of Honey Bees (Apis mellifera) Insects. 2017;8:22. doi: 10.3390/insects8010022. PubMed DOI PMC
Cianciosi D., Forbes-Hernández T.Y., Afrin S., Gasparrini M., Reboredo-Rodriguez P., Manna P.P., Zhang J., Bravo Lamas L., Martínez Flórez S., Agudo Toyos P. Phenolic Compounds in Honey and Their Associated Health Benefits: A Review. Molecules. 2018;23:2322. doi: 10.3390/molecules23092322. PubMed DOI PMC
Moniruzzaman M., Yung An C., Rao P.V., Hawlader M.N.I., Azlan S.A.B.M., Sulaiman S.A., Gan S.H. Identification of Phenolic Acids and Flavonoids in Monofloral Honey from Bangladesh by High Performance Liquid Chromatography: Determination of Antioxidant Capacity. BioMed Res. Int. 2014;2014:737490. doi: 10.1155/2014/737490. PubMed DOI PMC
Williams G.R., Alaux C., Costa C., Csaki T., Doublet V., Eisenhardt D., Brodschneider R. Standard Methods for Maintaining Adult Apis mellifera in Cages under in Vitro Laboratory Conditions. J. Apic. Res. 2013;52:1–36. doi: 10.3896/IBRA.1.52.1.04. DOI
Lourenço A.P., Mackert A., dos Santos Cristino A., Simões Z.L.P. Validation of Reference Genes for Gene Expression Studies in the Honey Bee, Apis mellifera, by Quantitative Real-Time RT-PCR. Apidologie. 2008;39:372–385. doi: 10.1051/apido:2008015. DOI
Livak K.J., Schmittgen T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-ΔΔCT Method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI
Mao W., Schuler M.A., Berenbaum M.R. CYP9Q-Mediated Detoxification of Acaricides in the Honey Bee (Apis mellifera) Proc. Natl. Acad. Sci. USA. 2011;108:12657–12662. doi: 10.1073/pnas.1109535108. PubMed DOI PMC
Calla B., MacLean M., Liao L., Dhanjal I., Tittiger C., Blomquist G.J., Berenbaum M.R. Functional Characterization of CYP4G11—a Highly Conserved Enzyme in the Western Honey Bee Apis mellifera. Insect Mol. Biol. 2018;27:661–674. doi: 10.1111/imb.12516. PubMed DOI
Tesovnik T., Cizelj I., Zorc M., Čitar M., Božič J., Glavan G., Narat M. Immune Related Gene Expression in Worker Honey Bee (Apis mellifera Carnica) Pupae Exposed to Neonicotinoid Thiamethoxam and Varroa Mites (Varroa Destructor) PLoS ONE. 2017;12:e0187079. doi: 10.1371/journal.pone.0187079. PubMed DOI PMC
Kaplan E.L., Meier P. Nonparametric Estimation from Incomplete Observations. J. Am. Stat. Assoc. 1958;53:457–481. doi: 10.1080/01621459.1958.10501452. DOI
Therneau T.M., Grambsch P.M. Modeling Survival Data: Extending the Cox Model. Springer; New York, NY, USA: 2000. The cox model; pp. 39–77.
Yu S.J. Interactions of Allelochemicals with Detoxication Enzymes of Insecticide-Susceptible and Resistant Fall Armyworms. Pestic. Biochem. Physiol. 1984;22:60–68. doi: 10.1016/0048-3575(84)90010-5. DOI
Mao W., Schuler M.A., Berenbaum M.R. Disruption of Quercetin Metabolism by Fungicide Affects Energy Production in Honey Bees (Apis mellifera) Proc. Natl. Acad. Sci. USA. 2017;114:2538–2543. doi: 10.1073/pnas.1614864114. PubMed DOI PMC
Porrini M.P., Fernández N.J., Garrido P.M., Gende L.B., Medici S.K., Eguaras M.J. In Vivo Evaluation of Antiparasitic Activity of Plant Extracts on Nosema Ceranae (Microsporidia) Apidologie. 2011;42:700–707. doi: 10.1007/s13592-011-0076-y. DOI
Tong L., Nieh J.C., Tosi S. Combined Nutritional Stress and a New Systemic Pesticide (Flupyradifurone, Sivanto®) Reduce Bee Survival, Food Consumption, Flight Success, and Thermoregulation. Chemosphere. 2019;237:124408. doi: 10.1016/j.chemosphere.2019.124408. PubMed DOI
Gregorc A., Alburaki M., Rinderer N., Sampson B., Knight P.R., Karim S., Adamczyk J. Effects of Coumaphos and Imidacloprid on Honey Bee (Hymenoptera: Apidae) Lifespan and Antioxidant Gene Regulations in Laboratory Experiments. Sci. Rep. 2018;8:15003. doi: 10.1038/s41598-018-33348-4. PubMed DOI PMC
Tosi S., Nieh J.C., Sgolastra F., Cabbri R., Medrzycki P. Neonicotinoid Pesticides and Nutritional Stress Synergistically Reduce Survival in Honey Bees. Proc. R. Soc. B. 2017;284:20171711. doi: 10.1098/rspb.2017.1711. PubMed DOI PMC
Manjon C., Troczka B.J., Zaworra M., Beadle K., Randall E., Hertlein G., Kumar S.S., Nauen R. Unravelling the Molecular Determinants of Bee Sensitivity to Neonicotinoid Insecticides. Curr. Biol. 2018;28:1137–1143. doi: 10.1016/j.cub.2018.02.045. PubMed DOI PMC
Alptekin S., Bass C., Nicholls C., Paine M.J., Clark S.J., Field L., Moores G.D. Induced Thiacloprid Insensitivity in Honeybees (Apis mellifera L.) Is Assoc. with Up-regulation of Detoxification Genes. Insect Mol. Biol. 2016;25:171–180. doi: 10.1111/imb.12211. PubMed DOI
Wheeler M.M., Robinson G.E. Diet-Dependent Gene Expression in Honey Bees: Honey vs. Sucrose or High Fructose Corn Syrup. Sci. Rep. 2014;4:5726. doi: 10.1038/srep05726. PubMed DOI PMC