Genersch, E. Honey bee pathology: Current threats to honey bees and beekeeping. Appl. Microbiol. Biotechnol. 87, 87–97. https://doi.org/10.1007/s00253-010-2573-8 (2010).
Google Scholar
Cameron, S. A. et al. Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. USA 108, 662–667. https://doi.org/10.1073/pnas.1014743108 (2011).
Google Scholar
Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, e0185809. https://doi.org/10.1371/journal.pone.0185809 (2017).
Google Scholar
Sánchez-Bayo, F. & Wyckhuys, K. A. G. Worldwide decline of the entomofauna: A review of its drivers. Biol. Conserv. 232, 8–27. https://doi.org/10.1016/j.biocon.2019.01.020 (2019).
Google Scholar
Goulson, D., Nicholls, E., Botias, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957. https://doi.org/10.1126/science.1255957 (2015).
Google Scholar
Vilcinskas, A. Pathogens associated with invasive or introduced insects threaten the health and diversity of native species. Curr. Opin. Insect. Sci. 33, 43–48. https://doi.org/10.1016/j.cois.2019.03.004 (2019).
Google Scholar
Sandrock, C. et al. Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure. PLoS ONE 9, e103592. https://doi.org/10.1371/journal.pone.0103592 (2014).
Google Scholar
Genersch, E. et al. The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41, 332–352. https://doi.org/10.1051/apido/2010014 (2010).
Google Scholar
Meixner, M. D. & Le Conte, Y. A current perspective on honey bee health. Apidologie 47, 273–275. https://doi.org/10.1007/s13592-016-0449-3 (2016).
Google Scholar
Desneux, N., Decourtye, A. & Delpuech, J. M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440 (2007).
Google Scholar
Retschnig, G. et al. Effects, but no interactions, of ubiquitous pesticide and parasite stressors on honey bee (Apis mellifera) lifespan and behaviour in a colony environment. Environ. Microbiol. 17, 4322–4331. https://doi.org/10.1111/1462-2920.12825 (2015).
Google Scholar
Rolke, D., Fuchs, S., Grünewald, B., Gao, Z. & Blenau, W. Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in Northern Germany: Effects on honey bees (Apis mellifera). Ecotoxicology 25, 1648–1665. https://doi.org/10.1007/s10646-016-1725-8 (2016).
Google Scholar
Woodcock, B. A. et al. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356, 1393–1395. https://doi.org/10.1126/science.aaa1190 (2017).
Google Scholar
Siede, R. et al. Performance of honey bee colonies under a long-lasting dietary exposure to sublethal concentrations of the neonicotinoid insecticide thiacloprid. Pest. Manag. Sci. 73, 1334–1344. https://doi.org/10.1002/ps.4547 (2017).
Google Scholar
Odemer, R., Nilles, L., Linder, N. & Rosenkranz, P. Sublethal effects of clothianidin and Nosema spp. on the longevity and foraging activity of free flying honey bees. Ecotoxicology 27, 527–538. https://doi.org/10.1007/s10646-018-1925-5 (2018).
Google Scholar
Han, P., Niu, C. Y., Lei, C. L., Cui, J. J. & Desneux, N. Use of an innovative T-tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera L. Ecotoxicology 19, 1612–1619. https://doi.org/10.1007/s10646-010-0546-4 (2010).
Google Scholar
Henry, M. et al. A common pesticide decreases foraging success and survival in honey bees. Science 336, 348–350. https://doi.org/10.1126/science.1215039 (2012).
Google Scholar
Decourtye, A. et al. Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pestic. Biochem. Physiol. 78, 83–92. https://doi.org/10.1016/j.pestbp.2003.10.001 (2004).
Google Scholar
Bartling, M. T., Vilcinskas, A. & Lee, K. Z. Sub-lethal doses of clothianidin inhibit the conditioning and biosensory abilities of the western honeybee Apis mellifera. Insects https://doi.org/10.3390/insects10100340 (2019).
Google Scholar
Yang, E. C., Chang, H. C., Wu, W. Y. & Chen, Y. W. Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS ONE 7, e49472. https://doi.org/10.1371/journal.pone.0049472 (2012).
Google Scholar
Alaux, C. et al. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12, 774–782. https://doi.org/10.1111/j.1462-2920.2009.02123.x (2010).
Google Scholar
Aufauvre, J. et al. Parasite-insecticide interactions: A case study of Nosema ceranae and fipronil synergy on honeybee. Sci. Rep. 2, 326. https://doi.org/10.1038/srep00326 (2012).
Google Scholar
Pettis, J. S., vanEngelsdorp, D., Johnson, J. & Dively, G. Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99, 153–158. https://doi.org/10.1007/s00114-011-0881-1 (2012).
Google Scholar
Doublet, V., Labarussias, M., de Miranda, J. R., Moritz, R. F. & Paxton, R. J. Bees under stress: Sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ. Microbiol. 17, 969–983. https://doi.org/10.1111/1462-2920.12426 (2015).
Google Scholar
Di Prisco, G. et al. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc. Natl. Acad. Sci. USA 110, 18466–18471. https://doi.org/10.1073/pnas.1314923110 (2013).
Google Scholar
Brochu, K. K. et al. Pollen defenses negatively impact foraging and fitness in a generalist bee (Bombus impatiens: Apidae). Sci. Rep. 10, 3112. https://doi.org/10.1038/s41598-020-58274-2 (2020).
Google Scholar
Daisley, B. A., Chmiel, J. A., Pitek, A. P., Thompson, G. J. & Reid, G. Missing microbes in bees: How systematic depletion of key symbionts erodes immunity. Trends Microbiol. https://doi.org/10.1016/j.tim.2020.06.006 (2020).
Google Scholar
Barribeau, S. M. et al. A depauperate immune repertoire precedes evolution of sociality in bees. Genome Biol. 16, 83. https://doi.org/10.1186/s13059-015-0628-y (2015).
Google Scholar
López-Uribe, M. M., Sconiers, W. B., Frank, S. D., Dunn, R. R. & Tarpy, D. R. Reduced cellular immune response in social insect lineages. Biol. Lett. 12, 20150984. https://doi.org/10.1098/rsbl.2015.0984 (2016).
Google Scholar
Berenbaum, M. R. & Johnson, R. M. Xenobiotic detoxification pathways in honey bees. Curr. Opin. Insect Sci. 10, 51–58. https://doi.org/10.1016/j.cois.2015.03.005 (2015).
Google Scholar
Lemaitre, B. & Hoffmann, J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697–743. https://doi.org/10.1146/annurev.immunol.25.022106.141615 (2007).
Google Scholar
Müller, U., Vogel, P., Alber, G. & Schaub, G. A. The innate immune system of mammals and insects. Contrib. Microbiol. 15, 21–44. https://doi.org/10.1159/000135684 (2008).
Google Scholar
Wilmes, M., Cammue, B. P., Sahl, H. G. & Thevissen, K. Antibiotic activities of host defense peptides: More to it than lipid bilayer perturbation. Nat. Prod. Rep. 28, 1350–1358. https://doi.org/10.1039/c1np00022e (2011).
Google Scholar
Wu, Q., Patocka, J. & Kuca, K. Insect antimicrobial peptides: A mini review. Toxins https://doi.org/10.3390/toxins10110461 (2018).
Google Scholar
Rahnamaeian, M. et al. Insect antimicrobial peptides show potentiating functional interactions against gram-negative bacteria. Proc. Biol. Sci. 282, 20150293. https://doi.org/10.1098/rspb.2015.0293 (2015).
Google Scholar
Rivero, A. Nitric oxide: An antiparasitic molecule of invertebrates. Trends Parasitol. 22, 219–225. https://doi.org/10.1016/j.pt.2006.02.014 (2006).
Google Scholar
Wink, D. A. & Mitchell, J. B. Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 25, 434–456. https://doi.org/10.1016/s0891-5849(98)00092-6 (1998).
Google Scholar
Gebicka, L. & Didik, J. Catalytic scavenging of peroxynitrite by catalase. J. Inorg. Biochem. 103, 1375–1379. https://doi.org/10.1016/j.jinorgbio.2009.07.011 (2009).
Google Scholar
Brunelli, L., Yermilov, V. & Beckman, J. S. Modulation of catalase peroxidatic and catalatic activity by nitric oxide. Free Radic. Biol. Med. 30, 709–714. https://doi.org/10.1016/s0891-5849(00)00512-8 (2001).
Google Scholar
Brunelli, L., Crow, J. P. & Beckman, J. S. The comparative toxicity of nitric oxide and peroxynitrite to Escherichia coli. Arch. Biochem. Biophys. 316, 327–334. https://doi.org/10.1006/abbi.1995.1044 (1995).
Google Scholar
Wells, P. G. et al. Glucuronidation and the UDP-glucuronosyltransferases in health and disease. Drug Metab. Dispos. 32, 281–290. https://doi.org/10.1124/dmd.32.3.281 (2004).
Google Scholar
Schmid, M. R., Brockmann, A., Pirk, C. W., Stanley, D. W. & Tautz, J. Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. J. Insect Physiol. 54, 439–444. https://doi.org/10.1016/j.jinsphys.2007.11.002 (2008).
Google Scholar
Wilson-Rich, N., Dres, S. T. & Starks, P. T. The ontogeny of immunity: Development of innate immune strength in the honey bee (Apis mellifera). J. Insect Physiol. 54, 1392–1399. https://doi.org/10.1016/j.jinsphys.2008.07.016 (2008).
Google Scholar
Bull, J. C. et al. A strong immune response in young adult honeybees masks their increased susceptibility to infection compared to older bees. PLoS Pathog 8, e1003083. https://doi.org/10.1371/journal.ppat.1003083 (2012).
Google Scholar
Suazo, A., Torto, B., Teal, P. E. A. & Tumlinson, J. H. Response of the small hive beetle (Aethina tumida) to honey bee (Apis mellifera) and beehive-produced volatiles. Apidologie 34, 525–533. https://doi.org/10.1051/apido:2003043 (2003).
Google Scholar
Lewis, K. A., Tzilivakis, J., Warner, D. J. & Green, A. An international database for pesticide risk assessments and management. Hum. Ecol. Risk Assess. 22, 1050–1064. https://doi.org/10.1080/10807039.2015.1133242 (2016).
Google Scholar
Schott, M. et al. Honeybee colonies compensate for pesticide-induced effects on royal jelly composition and brood survival with increased brood production. Sci. Rep. 11, 62. https://doi.org/10.1038/s41598-020-79660-w (2021).
Google Scholar
Crossthwaite, A. J. et al. The invertebrate pharmacology of insecticides acting at nicotinic acetylcholine receptors. J. Pestic. Sci. 42, 67–83. https://doi.org/10.1584/jpestics.D17-019 (2017).
Google Scholar
Liu, Y. J. et al. Thiacloprid exposure perturbs the gut microbiota and reduces the survival status in honeybees. J. Hazard Mater. 389, 121818. https://doi.org/10.1016/j.jhazmat.2019.121818 (2020).
Google Scholar
Vidau, C. et al. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 6, e21550. https://doi.org/10.1371/journal.pone.0021550 (2011).
Google Scholar
Dickel, F., Munch, D., Amdam, G. V., Mappes, J. & Freitak, D. Increased survival of honeybees in the laboratory after simultaneous exposure to low doses of pesticides and bacteria. PLoS ONE 13, e0191256. https://doi.org/10.1371/journal.pone.0191256 (2018).
Google Scholar
Mattson, M. P. Hormesis defined. Ageing Res. Rev. 7, 1–7. https://doi.org/10.1016/j.arr.2007.08.007 (2008).
Google Scholar
Pilling, E. D. & Jepson, P. C. Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera). Pestic. Sci. 39, 293–297. https://doi.org/10.1002/ps.2780390407 (1993).
Google Scholar
Neagu, A. et al. Expression signature of some immunity genes triggered in Apis mellifera carpatica model by Pseudomonas entomophila experimental infection. Roum. Arch. Microbiol. Immunol. 18, 18–24 (2016).
Bogdan, C., Rollinghoff, M. & Diefenbach, A. The role of nitric oxide in innate immunity. Immunol. Rev. 173, 17–26. https://doi.org/10.1034/j.1600-065x.2000.917307.x (2000).
Google Scholar
DeGrandi-Hoffman, G. & Chen, Y. Nutrition, immunity and viral infections in honey bees. Curr. Opin. Insect Sci. 10, 170–176. https://doi.org/10.1016/j.cois.2015.05.007 (2015).
Google Scholar
Zhao, J. Interplay among nitric oxide and reactive oxygen species: A complex network determining cell survival or death. Plant Signal Behav. 2, 544–547. https://doi.org/10.4161/psb.2.6.4802 (2007).
Google Scholar
Sadekuzzaman, M., Stanley, D. & Kim, Y. Nitric Oxide mediates insect cellular immunity via Phospholipase A2 activation. J. Innate Immun. 10, 70–81. https://doi.org/10.1159/000481524 (2018).
Google Scholar
Nappi, A. J., Vass, E., Frey, F. & Carton, Y. Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4, 423–430. https://doi.org/10.1006/niox.2000.0294 (2000).
Google Scholar
Kim, S. H. & Lee, W. J. Role of DUOX in gut inflammation: Lessons from Drosophila model of gut-microbiota interactions. Front. Cell. Infect. Microbiol. 3, 116. https://doi.org/10.3389/fcimb.2013.00116 (2014).
Google Scholar
Ha, E. M., Oh, C. T., Bae, Y. S. & Lee, W. J. A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847–850. https://doi.org/10.1126/science.1117311 (2005).
Google Scholar
Chmiel, J. A., Daisley, B. A., Burton, J. P. & Reid, G. Deleterious effects of neonicotinoid pesticides on Drosophila melanogaster immune pathways. mBio https://doi.org/10.1128/mBio.01395-19 (2019).
Google Scholar
Ozcan, A. & Ogun, M. Biochemistry of reactive oxygen and nitrogen species. Basic Princ. Clin. Signif. Oxid. Stress https://doi.org/10.5772/61193 (2015).
Google Scholar
Sadekuzzaman, M. & Kim, Y. Nitric oxide mediates antimicrobial peptide gene expression by activating eicosanoid signaling. PLoS ONE 13, e0193282. https://doi.org/10.1371/journal.pone.0193282 (2018).
Google Scholar
Foley, E. & O’Farrell, P. H. Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes Dev. 17, 115–125. https://doi.org/10.1101/gad.1018503 (2003).
Google Scholar
Hsieh, H. J., Liu, C. A., Huang, B., Tseng, A. H. & Wang, D. L. Shear-induced endothelial mechanotransduction: The interplay between reactive oxygen species (ROS) and nitric oxide (NO) and the pathophysiological implications. J. Biomed. Sci. 21, 3. https://doi.org/10.1186/1423-0127-21-3 (2014).
Google Scholar
Lee, K. A. et al. Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 153, 797–811. https://doi.org/10.1016/j.cell.2013.04.009 (2013).
Google Scholar
Negri, P. et al. Nitric oxide participates at the first steps of Apis mellifera cellular immune activation in response to non-self recognition. Apidologie 44, 575–585. https://doi.org/10.1007/s13592-013-0207-8 (2013).
Google Scholar
Negri, P. et al. Apis mellifera hemocytes generate increased amounts of nitric oxide in response to wounding/encapsulation. Apidologie 45, 610–617. https://doi.org/10.1007/s13592-014-0279-0 (2014).
Google Scholar
Mehta, S. K. & Gowder, S. J. T. Members of antioxidant machinery and their functions. IntechOpen. https://doi.org/10.5772/61884 (2015).
Google Scholar
Werck-Reichhart, D. & Feyereisen, R. Cytochromes P450: A success story. Genome. Biol. https://doi.org/10.1186/gb-2000-1-6-reviews3003 (2000).
Google Scholar
Anzenbacher, P. & Anzenbacherova, E. Cytochromes P450 and metabolism of xenobiotics. Cell Mol. Life Sci. 58, 737–747. https://doi.org/10.1007/pl00000897 (2001).
Google Scholar
Manjon, C. et al. Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Curr. Biol. 28, 1137–1143. https://doi.org/10.1016/j.cub.2018.02.045 (2018).
Google Scholar
Thimmegowda, G. G. et al. A field-based quantitative analysis of sublethal effects of air pollution on pollinators. Proc. Natl. Acad. Sci. U S A 117, 20653–20661. https://doi.org/10.1073/pnas.2009074117 (2020).
Google Scholar
Zheng, L. et al. Transcriptomic analysis reveals importance of ROS and phytohormones in response to short-term salinity stress in Populus tomentosa. Front. Plant Sci. 6, 678. https://doi.org/10.3389/fpls.2015.00678 (2015).
Google Scholar
Jiang, J., Shi, Y., Yu, R., Chen, L. & Zhao, X. Biological response of zebrafish after short-term exposure to azoxystrobin. Chemosphere 202, 56–64. https://doi.org/10.1016/j.chemosphere.2018.03.055 (2018).
Google Scholar
Rodrigues, N. R. et al. Short-term sleep deprivation with exposure to nocturnal light alters mitochondrial bioenergetics in Drosophila. Free Radic. Biol. Med. 120, 395–406. https://doi.org/10.1016/j.freeradbiomed.2018.04.549 (2018).
Google Scholar
Brandt, A. et al. Immunosuppression response to the neonicotinoid insecticide thiacloprid in females and males of the red mason bee Osmia bicornis L. Sci. Rep. 10, 4670. https://doi.org/10.1038/s41598-020-61445-w (2020).
Google Scholar
Brandt, A. et al. Immunosuppression in honeybee queens by the neonicotinoids thiacloprid and clothianidin. Sci. Rep. 7, 4673. https://doi.org/10.1038/s41598-017-04734-1 (2017).
Google Scholar
Brandt, A., Gorenflo, A., Siede, R., Meixner, M. & Buchler, R. The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). J. Insect Physiol. 86, 40–47. https://doi.org/10.1016/j.jinsphys.2016.01.001 (2016).
Google Scholar
Schlüns, H. & Crozier, R. H. Relish regulates expression of antimicrobial peptide genes in the honeybee, Apis mellifera, shown by RNA interference. Insect Mol. Biol. 16, 753–759. https://doi.org/10.1111/j.1365-2583.2007.00768.x (2007).
Google Scholar
Carreck, N. L. & Ratnieks, F. L. W. The dose makes the poison: Have “field realistic” rates of exposure of bees to neonicotinoid insecticides been overestimated in laboratory studies?. J. Apic. Res. 53, 607–614. https://doi.org/10.3896/ibra.1.53.5.08 (2015).
Google Scholar
Schott, M. et al. Temporal dynamics of whole body residues of the neonicotinoid insecticide imidacloprid in live or dead honeybees. Sci. Rep. 7, 6288. https://doi.org/10.1038/s41598-017-06259-z (2017).
Google Scholar
Cullen, M. G., Thompson, L. J., Carolan, J. C., Stout, J. C. & Stanley, D. A. Fungicides, herbicides and bees: A systematic review of existing research and methods. PLoS ONE 14, e0225743. https://doi.org/10.1371/journal.pone.0225743 (2019).
Google Scholar
Han, J. et al. Marine copepod cytochrome P450 genes and their applications for molecular ecotoxicological studies in response to oil pollution. Mar. Pollut. Bull. 124, 953–961. https://doi.org/10.1016/j.marpolbul.2016.09.048 (2017).
Google Scholar
Regoli, F. et al. Oxidative stress in ecotoxicology: From the analysis of individual antioxidants to a more integrated approach. Mar. Environ. Res. 54, 419–423. https://doi.org/10.1016/s0141-1136(02)00146-0 (2002).
Google Scholar
Sheehan, G., Farrell, G. & Kavanagh, K. Immune priming: The secret weapon of the insect world. Virulence 11, 238–246. https://doi.org/10.1080/21505594.2020.1731137 (2020).
Google Scholar
Therneau, T. A Package for Survival Analysis in R. R package version 3.2–7. (2020).
Source: Ecology - nature.com
