Bees under stress: Sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle

Environmental Microbiology

Volumn 17, Issue 4, 2015, Pages 969-983

  Doublet, Vincent ^a,e   Labarussias, Maureen ^a   de Miranda, Joachim R ^b   Moritz, Robin F A ^a,c   Paxton, Robert J ^a,c,d  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

^d QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^e Synthesis Centre for Biodiversity Sciences   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APIS MELLIFERA; APOIDEA; BLACK QUEEN CELL VIRUS; HEXAPODA; NOSEMA CERANAE;

PESTICIDE; PYRIDINE DERIVATIVE; THIACLOPRID; THIAZINE DERIVATIVE;

ANIMAL; BEE; DICISTROVIRIDAE; DRUG EFFECTS; LARVA; LIFE CYCLE STAGE; MICROBIOLOGY; NOSEMA; PATHOGENICITY; VIROLOGY;

ANIMALS; BEES; DICISTROVIRIDAE; LARVA; LIFE CYCLE STAGES; NOSEMA; PESTICIDES; PYRIDINES; THIAZINES;

EID: 84926419601     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12426     Document Type: Article

References (91)

1. Alaux, C., Brunet, J.-L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., etal. (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol 12: 774-782.
2. Aliouane, Y., El Hassani, A.K., Gary, V., Armengaud, C., Lambin, M., and Gauthier, M. (2009) Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior. Environ Toxicol Chem 28: 113-122.
3. Aupinel, P., Fortini, D., Dufour, H., Tasei, J.-N., Michaud, B., Odoux, J.-F., and Pham-Delègue, M.-H. (2005) Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bull Insectology 58: 107-111.
4. Bailey, L., and Ball, B.V. (1991) Honey Bee Pathology, 2nd edn. London, UK: Academc Press.
5. Bailey, L., and Woods, R.D. (1977) Two more small RNA viruses from honey bees and further observations on sacbrood and acute bee-paralysis viruses. J Gen Virol 37: 175-182.
6. Bailey, L., Ball, B.V., and Perry, J.N. (1983) Association of viruses with two protozoal pathogens of the honey bee. Ann Appl Biol 103: 13-20.
7. Bartomeus, I., Ascher, J.S., Gibbs, J., Danforth, B.N., Wagner, D.L., Hedtke, S.M., and Winfree, R. (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc Natl Acad Sci USA 110: 4656-4660.
8. Bartoń, K. (2013) MuMIn: multi-model inference. R package ver 1.9.0.
9. Bauer, L.S., Miller, D.L., Maddox, J.V., and McManus, M.L. (1998) Interactions between a Nosema sp. (Microspora: nosematidae) and nuclear polyhedrosis virus infecting the gypsy moth, Lymantria dispar (Lepidoptera: lymantriidae). J Invertebr Pathol 72: 147-153.
10. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., etal. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313: 351-354.
11. Bommarco, R., Lundin, O., Smith, H.G., and Rundlöf, M. (2012) Drastic historic shifts in bumble-bee community composition in Sweden. Proc R Soc Lond B 279: 309-315.
12. Boncristiani, H., Underwood, R., Schwarz, R., Evans, J.D., Pettis, J., and vanEngelsdorp, D. (2012) Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. J Insect Physiol 58: 613-620.
13. Bromenshenk, J.J., Henderson, C.B., Wick, C.H., Stanford, M.F., Zulich, A.W., Jabbour, R.E., etal. (2010) Iridovirus and microsporidian linked to honey bee colony decline. PLoS ONE 5: e13181.
14. Burkle, L.A., Marlin, J.C., and Knight, T.M. (2013) Plant-pollinator interactions over 120 years: loss os species, co-occurrence and function. Science 339: 1611-1615.
15. Cameron, S.A., Lozier, J.D., Strange, J.P., Koch, J.B., Cordes, N., Solter, L.F., and Griswold, T.L. (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci USA 108: 662-667.
16. Chen, Y., Evans, J., and Feldlaufer, M. (2006) Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J Invertebr Pathol 92: 152-159.
17. Chen, Y.-P., and Siede, R. (2007) Honey bee viruses. Adv Virus Res 70: 33-80.
18. Cornman, R.S., Tarpy, D.S., Chen, Y., Jeffreys, L., Lopez, D., Pettis, J.S., etal. (2012) Pathogen webs in collapsing honey bee colonies. PLoS ONE 7: e43562.
19. Cox-Foster, D.L., Conlan, S., Holmes, E.C., Palacios, G., Evans, J.D., Moran, N.A., etal. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287.
20. Crailsheim, K. (1990) The protein balance of the honey bee worker. Apidologie 21: 417-429.
21. Crailsheim, K., Brodschneider, R., Aupinel, P., Behrens, D., Genersch, E., Vollmann, J., and Reissberger-Gallé, U. (2013) Standard methods for artificial rearing of Apis mellifera larvae. In The COLOSS BEEBOOK, Vol. I. Dietemann, V., Ellis, J.D., and Neumann, P. (eds). Standard methods for Apis mellifera research. J Apic Res 52(1).
22. Dai, P.-L., Wang, Q., Sun, J.-H., Liu, F., Wang, X., Wu, Y.-Y., and Zhou, T. (2010) Effects of sublethal concentrations of bifenthrin and deltamethrin on fecundity, growth, and development of the honeybee Apis mellifera ligustica. Environ Toxicol Chem 29: 644-649.
23. Dainat, B., Evans, J.D., Chen, Y.P., Gauthier, L., and Neumann, P. (2012) Predictive markers of honey bee colony collapse. PLoS ONE 7: e32151.
24. Decourtye, A., Armengaud, C., Renou, M., Devillers, J., Cluzeau, S., Gauthier, M., and Pham-Delègue, M.-H. (2004) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pestic Biochem Physiol 78: 83-92.
25. Decourtye, A., Devillers, J., Genecque, E., Le Menach, K., Budzinski, H., Cluzeau, S., and Pham-Delègue, M. (2005) Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch Environ Contam Toxicol 48: 242-250.
26. Decourtye, A., Lefort, S., Devillers, J., Gauthier, M., Aupinel, P., and Tisseur, M. (2009) Sublethal effects of fipronil on the ability of honeybees (Apis mellifera L.) to orientate in a complex maze. Julius-Kühn-Archiv 423: 75-83.
27. Di Prisco, G., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F., etal. (2013) Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc Natl Acad Sci USA 110: 18466-18471.
28. Elston, C., Thompson, H.M., and Walters, K.F.A. (2013) Sub-lethal effects of thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (Bombus terrestris) micro-colonies. Apidologie 44: 563-574.
29. Evans, J.D., and Schwarz, R.S. (2011) Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol 19: 614-620.
30. Fluri, P., Lüscher, M., Willf, H., and Gerig, L. (1982) Changes in weight of the pharyngeal gland and haemolymph titres of juvenile hormone, protein and vitellogenin in worker honey bee. J Insect Physiol 28: 61-68.
31. Francis, R.M., Nielsen, S.L., and Kryger, P. (2013) Varroa-virus interaction in collapsing honey bee colonies. PLoS ONE 8: e57540.
32. Fries, I. (2010) Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 103: S73-S79.
33. Fries, I., and Camazine, S. (2001) Implications of horizontal and vertical pathogen transmission for honey bee epidemiology. Apidologie 32: 199-214.
34. Fries, I., Chauzat, M.-P., Chen, Y.-P., Doublet, V., Genersch, E., Gisder, S., etal. (2013) Standard methods for Nosema research. In The COLOSS BEEBOOK, Vol. I. Dietemann, V., Ellis, J.D., and Neumann, P. (eds). Standard methods for Apis mellifera research. J Apic Res 52(1).
35. Frost, E.H., Shutler, D., and Hillier, N.K. (2013) Effects of fluvalinate on honey bee learning, memory, responsiveness to sucrose, and survival. J Exp Biol 216: 2931-2938.
36. Gallai, N., Salles, J.-M., Settele, J., and Vaissière, B.E. (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68: 810-821.
37. Gill, R.J., Ramos-Rodriguez, O., and Raine, N.E. (2012) Combined pesticide exposure severely affects individual and colonylevel traits in bees. Nature 491: 105-108.
38. González-Varo, J.P., Biesmeijer, J.C., Bommarco, R., Potts, S.G., Schweiger, O., Smith, H.G., etal. (2013) Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol 28: 524-530.
39. Ha, I.D., Noh, M., and Lee, Y. (2012) frailtyHL: Frailty Models via H-likelihood. R package, ver. 1.1. In.
40. Harris, J.W., and Woodring, J. (1992) Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honey bee (Apis mellifera L.) brain. J Insect Physiol 38: 29-35.
41. Henry, M., Béguin, M., Requier, F., Rollin, O., Odoux, J.-F., Aupinel, P., etal. (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336: 348-350.
42. Higes, M., Martin-Hernández, R., Botías, C., Garrido Bailón, E., González-Porto, A.M., Barrios, L., etal. (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10: 2659-2669.
43. Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A.V., García-Palencia, P., Meana, A., etal. (2009) Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ Microbiol Rep 1: 110-113.
44. Higes, M., Meana, A., Bartolomé, C., Botías, C., and Martín-Hernández, R. (2013) Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol Rep 5: 17-29.
45. Hoover, S.E.R., Higo, H.A., and Winston, M.L. (2006) Worker honey bee ovary development: seasonal variation and the influence of larval and adult nutrition. J Comp Physiol B 176: 55-63.
46. Hothorn, T., Bretz, F., Westfal, P., Heiberger, R.M., and Schuetzenmeister, A. (2013) multcomp: simultaneous inference in general parametric models. R package ver. 1.2-15. In.
47. Huang, Z.-Y., and Robinson, G.E. (1995) Seasonal changes in juvenile hormone titers and rates of biosynthesis in honey bees. J Comp Physiol B 165: 18-28.
48. Iwasa, T., Motoyama, N., Ambrose, J.T., and Roe, R.M. (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot 23: 371-378.
49. Johnson, R.M., Pollock, H.S., and Berenbaum, M.R. (2009a) Synergistic interactions between in-hive miticides in Apis mellifera. J Econ Entomol 102: 474-479.
50. Johnson, R.M., Evans, J.D., Robinson, G.E., and Berenbaum, M.R. (2009b) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proc Natl Acad Sci USA 106: 14790-14795.
51. Johnson, R.M., Dahlgren, L., Siegfried, B.D., and Ellis, M.D. (2013) Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLoS ONE 8: e54092.
52. Klee, J., Besana, A.M., Genersch, E., Gisder, S., Nanetti, A., Tam, D.Q., etal. (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96: 1-10.
53. Klein, A.-M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., and Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond B 274: 303-313.
54. Laurino, D., Poprporato, M., Patetta, A., and Manino, A. (2011) Toxicity of neonicotinoid insecticides to honey bees: laboratory tests. Bull Insectology 64: 107-113.
55. Locke, B., Forsgren, E., Fries, I., and de Miranda, J.R. (2012) Acaricide treatment affects viral dynamics in Varroa destructor-infested honey bee colonies via both host physiology and mite control. Appl Environ Microbiol 78: 227-235.
56. Martín-Hernández, R., Botías, C., Barrios, L., Martínez-Salvador, A., Meana, A., Mayack, C., and Higes, M. (2011) Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitol Res 3: 605-612.
57. Mayack, C., and Naug, D. (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol 100: 185-188.
58. Medrzycki, P., Montanari, R., Bortolotti, L., Sabatini, A.G., Maini, S., and Porrini, C. (2003) Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests. Bull Insectology 56: 59-62.
59. de Miranda, J.R., Bailey, L., Ball, B.V., Blanchard, P., Budge, G.E., Chejanovsky, N., etal. (2013) Standard methods for virus research in Apis mellifera. In The COLOSS BEEBOOK, Vol. II. Dietemann, V., Ellis, J.D., and Neumann, P. (eds). Standard methods for Apis mellifera research. J Apic Res 52(4).
60. Nazzi, F., Brown, S.P., Annoscia, D., Del Piccolo, F., Di Prisco, G., Varricchio, P., etal. (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 8: e1002735.
61. Neumann, P., and Carreck, N.L. (2010) Honey bee colony losses. J Apic Res 49: 1-6.
62. Palmer, M.J., Moffat, C., Saranzewa, N., Harvey, J., Wright, G.A., and Conolly, C.N. (2013) Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nat Commun 4: 1634.
63. Paxton, R.J. (2010) Does infection by Nosema ceranae cause 'Colony Collapse Disorder' in honey bees (Apis mellifera)? J Apic Res 49: 80-84.
64. Paxton, R.J., Klee, J., Korpela, S., and Fries, I. (2007) Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38: 1-9.
65. Pettis, J.S., vanEngelsdorp, D., Johnson, J., and Dively, G. (2012) Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99: 153-158.
66. Pilling, E.D., and Jepson, P.C. (1993) Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera). Pestic Sci 39: 293-297.
67. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., and Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25: 345-353.
68. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, V., Austria. ISBN 3-900051-07-0. URL http://www.R-project.org.
69. Ramirez-Romero, R., Chaufaux, J., and Pham-Delègue, M.-H. (2005) Effects of Cry1Ab protoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee Apis mellifera, a comparative approach. Apidologie 36: 601-611.
70. Ratnieks, L.W., and Carreck, N.L. (2010) Clarity on honey bee collapse? Science 327: 152-153.
71. Ravoet, J., Maharramov, J., Meeus, I., De Smet, L., Wenseleers, T., Smagghe, G., and de Graaf, D.C. (2013) Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PLoS ONE 8: e72443.
72. Ray, S., and Ferneyhough, B. (1997) Seasonal variation of proboscis extension reflex conditioning in the honey bee (Apis mellifera). J Apic Res 36: 108-110.
73. Schmid-Hempel, P. (1998) Parasites in Social Insects. Princeton, New Jersey, USA: Princeton University Press.
74. Schneider, C.W., Tautz, J., Grünewald, B., and Fuchs, S. (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS ONE 7: e30023.
75. Singh, R., Levitt, A.L., Rajotte, E.G., Holmes, E.C., Ostiguy, N., vanEngelsdorp, D., etal. (2010) RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS ONE 5: e14357.
76. Smodiš Škerl, M.I., Velikonja Bolta, Š., Baša Česnik, H., and Gregorc, A. (2009) Residues of pesticides in honeybee (Apis mellifera carnica) bee bread and in pollen loads from treated apple orchards. Bull Environ Contam Toxicol 83: 374-377.
77. Suchail, S., Guez, D., and Belzunces, L.P. (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem 20: 2482-2486.
78. Therneau, T. (2012) coxme: Mixed effects Cox models. R package ver 2.2-3.
79. Toplak, I., Ciglenečki, U.J., Aronstein, K., and Gregorc, A. (2013) Chronic bee paralysis virus and Nosema ceranae experimental co-infection of winter honey bee workers (Apis mellifera L.). Viruses 5: 2282-2297.
80. Traver, B.E., Williams, M.R., and Fell, R.D. (2012) Comparison of within hive sampling and seasonal activity of Nosema ceranae in honey bee colonies. J Invertebr Pathol 109: 187-193.
81. vanEngelsdorp, D., Caron, D., Hayes, J., Underwood, R., Henson, M., Rennich, K., etal. (2012) A national survey of managed honey bee 2010-11 winter colony losses in the USA: results from the Bee Informed Partnership. J Apic Res 51: 115-124.
82. Vanbergen, A.J., and The Insect Pollinators Initiative (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11: 251-259.
83. Vidau, C., Diogon, M., Aufauvre, J., Fontbonne, R., Viguès, B., Brunet, J.-L., etal. (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 6: e21550.
84. Whitehorn, P.R., O'Connor, S., Wackers, F., and Goulson, D. (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336: 351-352.
85. Williams, G.R., Alaux, C., Costa, C., Csáki, T., Doublet, V., Eisenhardt, D., etal. (2013) Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. In The COLOSS BEEBOOK, Vol. I. Dietemann, V., Ellis, J.D., and Neumann, P. (eds). Standard methods for Apis mellifera research. J Apic Res 52(1).
86. Williamson, S.M., and Wright, G.A. (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 216: 1799-1807.
87. Williamson, S.M., Moffat, C., Gormesall, M.A.E., Saranzewa, N., Conolly, C.N., and Wright, G.A. (2013) Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees. Front Physiol 4: 13.
88. Wu, J.Y., Anelli, C.M., and Sheppard, W.S. (2011) Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS ONE 6: e14720.
89. Wu, J.Y., Smart, M.D., Anelli, C.M., and Sheppard, W.S. (2012) Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. J Invertebr Pathol 109: 326-329.
90. Yang, E.-C., Chang, H.-C., Wu, W.-Y., and Chen, Y.-W. (2012) Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS ONE 7: e49472.
91. Yang, E.C., Chuang, Y.C., Chen, Y.L., and Chang, L.H. (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 101: 1743-1748.