Flight behavior and pheromone changes associated to Nosema ceranae infection of honey bee workers (Apis mellifera) in field conditions

Journal of Invertebrate Pathology

Volumn 113, Issue 1, 2013, Pages 42-51

  Dussaubat, Claudia ^a   Maisonnasse, Alban ^a,d   Crauser, Didier ^a   Beslay, Dominique ^a   Costagliola, Guy ^b   Soubeyrand, Samuel ^c   Kretzchmar, André ^c   Le Conte, Yves ^a  

^a Laboratoire de Toxicologie Environnementale   (France)

^b Domaine Saint Paul   (France)

^c INRA   (France)

^d Maison des Agriculteurs 22   (France)

Author keywords

Apis mellifera; Colony losses; Ethyl oleate; Flight behavior; Host parasite interactions; Nosema ceranae

Indexed keywords

PHEROMONE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BEE; COLONY COLLAPSE; FLYING; HOST PARASITE INTERACTION; METABOLISM; MICROBIOLOGY; NOSEMA; PHYSIOLOGY; SOCIAL BEHAVIOR;

ANIMALS; BEES; BEHAVIOR, ANIMAL; COLONY COLLAPSE; FLIGHT, ANIMAL; HOMING BEHAVIOR; HOST-PARASITE INTERACTIONS; NOSEMA; PHEROMONES; SOCIAL BEHAVIOR;

EID: 84873715117     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2013.01.002     Document Type: Article

References (65)

1. Alaux, C., Brunet, J.L., Dussaubat, C., Mondet, F., Tchamitchan, S., Cousin, M., Brillard, J., Baldy, A., Belzunces, L.P., Conte, Y.L., Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ. Microbiol. 12 (2010), 774–782.
2. Aliferis, K.A., Copley, T., Jabaji, S., Gas chromatography–mass spectrometry metabolite profiling of worker honey bee (Apis mellifera L.) hemolymph for the study of Nosema ceranae infection. J. Insect Physiol. 58 (2012), 1349–1359.
3. Antúnez, K., Martín-Hernández, R., Prieto, L., Meana, A., Zunino, P., Higes, M., Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ. Microbiol. 11 (2009), 2284–2290.
4. Ares, A.M., Nozal, M.J., Bernal, J.L., Martín-Hernández, R., Higes, M., Bernal, J., Liquid chromatography coupled to ion trap-tandem mass spectrometry to evaluate juvenile hormone III levels in bee hemolymph from Nosema spp. infected colonies. J. Chromatogr. B 899 (2012), 146–153.
5. Bailey, L., Fernando, E.F.W., Effects of sacbrood virus on adult honeybees. Ann. Appl. Biol. 72 (1972), 27–35.
6. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemuller, R., Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J., Kunin, W.E., Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313 (2006), 351–354.
7. Botías, C., Martín-Hernández, R., Días, J., García-Palencia, P., Matabuena, M., Juarranz, A., Barrios, L., Meana, A., Nanetti, A., Higes, M., The effect of induced queen replacement on Nosema spp. infection in honey bee (Apis mellifera iberiensis) colonies. Environ. Microbiol. 14 (2012), 845–859.
8. Calderone, N.W., Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992–2009. Plos One, 7, 2012, e37235.
9. Castillo, C., Maisonnasse, A., Conte, Y.L., Plettner, E., Seasonal variation in the titers and biosynthesis of the primer pheromone ethyl oleate in honey bees. J. Insect Physiol. 58 (2012), 1112–1121.
10. Chaimanee, V., Chantawannakul, P., Chen, Y., Evans, J.D., Pettis, J.S., Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. J. Insect Physiol. 58 (2012), 1090–1095.
11. Chen, Y., Evans, J.D., Smith, I.B., Pettis, J.S., Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. J. Invertebr. Pathol. 97 (2008), 186–188.
12. Dussaubat, C., Maisonnasse, A., Alaux, C., Tchamitchan, S., Brunet, J.L., Plettner, E., Belzunces, L.P., Le Conte, Y., Nosema spp. infection alters pheromone production in honey bees (Apis mellifera). J. Chem. Ecol. 36 (2010), 522–525.
13. Dussaubat, C., Brunet, J.L., Higes, M., Colbourne, J.K., Lopez, J., Jeong-Hyeon, C., Martín-Hernández, R., Botías, C., Cousin, M., McDonnell, C., Bonnet, M., Belzunces, L.P., Moritz, R.F.A., Le Conte, Y., Alaux, C., Gut pathology and responses to the Microsporidium Nosema ceranae in the honey bee Apis mellifera. Plos One, 7, 2012, e37017.
14. Evans, J.D., Spivak, M., Socialized medicine: individual and communal disease barriers in honey bees. J. Invertebr. Pathol. 103 (2010), S62–S72.
15. Fernández, J.M., Puerta, F., Cousinou, M., Dios-Palomares, R., Campano, F., Redondo, L., Asymptomatic presence of Nosema spp. in Spanish commercial apiaries. J. Invertebr. Pathol. 111 (2012), 106–110.
16. Forsgren, E., Fries, I., Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet. Parasitol. 170 (2010), 212–217.
17. Fries, I., Comb replacement and Nosema disease (Nosema apis Z) in honey bee colonies. Apidologie 19 (1988), 343–354.
18. Fries, I., Feng, F., daSilva, A., Slemenda, S.B., Pieniazek, N.J., Nosema ceranae n sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur. J. Protist. 32 (1996), 356–365.
19. Fries, I., Martín-Hernández, R., Meana, A., García-Palencia, P., Higes, M., Natural infections of Nosema ceranae in European honey bees. J. Apicult. Res. 45 (2006), 230–233.
20. Gallai, N., Salles, J.M., Settele, J., Vaissiere, B.E., Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68 (2009), 810–821.
21. Giray, T., Robinson, G.E., Effects of intracolony variability in behavioral development on plasticity of division of labor in honey bee colonies. Behav. Ecol. Sociobiol. 35 (1994), 13–20.
22. Hassanein, M.H., The influence of infection with Nosema apis on the activities and longevity of the worker honeybee. Ann. App. Biol. 40 (1953), 418–423.
23. Heinze, J., Walter, B., Moribund ants leave their nests to die in social isolation. Curr. Biol. 20 (2010), 249–252.
24. Higes, M., Martín-Hernández, R., Meana, A., Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J. Invertebr. Pathol. 92 (2006), 93–95.
25. Higes, M., García-Palencia, P., Martín-Hernández, R., Meana, A., Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J. Invertebr. Pathol. 94 (2007), 211–217.
26. Higes, M., Martín-Hernández, R., Botías, C., Garrido Bailón, E., González-Porto, A.V., Barrios, L., del Nozal, M.J., Bernal, J.L., Jiménez, J.J., García Palencia, P., Meana, A., How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 10 (2008), 2659–2669.
27. Higes, M., Martín-Hernández, R., Martínez-Salvador, A., Garrido-Bailón, E., González-Porto, A.V., Meana, A., Bernal, J.L., del Nozal, M.J., Bernal, J., A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environ. Microbiol. Rep. 2 (2009), 243–250.
28. Huang, Z.Y., Lin, R., JH titers, biosynthesis and metabolism in honey bee workers infected by a microsporidia parasite, Nosema apis. J. Insect Sci., 4, 2004, 7.
29. Huang, W.F., Jiang, J.H., Chen, Y.W., Wang, C.H., A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38 (2007), 30–37.
30. Iqbal, J., Mueller, U., Virus infection causes specific learning deficits in honeybee foragers. Proc. R. Soc. Bullet. Biol. Sci. 274 (2007), 1517–1521.
31. Khoury, D.S., Myerscough, M.R., Barron, A.B., A quantitative model of honey bee colony population dynamics. Plos One, 6(4), 2011, e18491.
32. Klee, J., Besana, A.M., Genersch, E., Gisder, S., Nanetti, A., Tam, D.Q., Chinh, T.X., Puerta, F., Ruz, J.M., Kryger, P., Message, D., Hatjina, F., Korpela, S., Fries, I., Paxton, R.J., Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invertebr. Pathol. 96 (2007), 1–10.
33. Klein, A.M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunnigham, S.A., Kremen, C., Tscharntke, T., Importance of pollinators in changing landscapes for world crops. P. Roy. Soc. 274 (2007), 303–313.
34. Kralj, J., Fuchs, S., Parasitic Varroa destructor mites influence flight duration and homing ability of infested Apis mellifera foragers. Apidologie 37 (2006), 577–587.
35. Kralj, J., Fuchs, S., Nosema sp. influences flight behavior of infected honey bee (Apis mellifera) foragers. Apidologie 41 (2010), 21–28.
36. Lautenbach, S., Seppelt, R., Liebscher, J., Dormann, C.F., Spatial and temporal trends of global pollination benefit. Plos One, 7(4), 2012, e35954.
37. Leoncini, I., Le Conte, Y., Costagliola, G., Plettner, E., Toth, A.L., Wang, M.W., Huang, Z., Becard, J.M., Crauser, D., Slessor, K.N., Robinson, G.E., Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. PNAS 101 (2004), 17559–17564.
38. Lin, H., Sullivan, J., Huang, Z.Y., 2009. Mechanisms through which Nosema apis affects onset of foraging in worker honeybees (Apis mellifera L.). In: Nosema disease: Lack of Knowledge and Work Standardization. Prevention of Honeybee COlony LOSSes, COST Action FA0803, Guadalajara, Spain, 19–22 October, < http://www.coloss.org/publications/Nosema-Workshop-Proceedings.pdf>.
39. Malone, L.A., Gatehouse, H.S., Effects of Nosema apis infection on honey bee (Apis mellifera) digestive proteolytic enzyme activity. J. Invertebr. Pathol. 71 (1998), 169–174.
40. Mayack, C., Naug, D., Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J. Invertebr. Pathol. 100 (2009), 185–188.
41. Mayack, C., Naug, D., Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. J. Insect Physiol. 56 (2010), 1572–1575.
42. McCullagh, P., Nelder, J.A., Generalized Linear Models. second ed., 1989, Chapman & Hall, London.
43. Miller, R.G. Jr., Simultaneous Statistical Inference. 1981, Springer-Verlag, New York.
44. Naug, D., Camazine, S., The role of colony organization on pathogen transmission in social insects. J. Theor. Biol. 215 (2002), 427–439.
45. Naug, D., Gibbs, A., Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae. Apidologie 40 (2009), 595–599.
46. 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 (2012), 153–158.
47. Paxton, R.J., Does infection by Nosema ceranae cause “Colony Collapse Disorder” in honey bees (Apis mellifera)?. J. Apicult. Res. 49 (2010), 80–84.
48. Ratnieks, F.L.W., Carreck, N.L., Clarity on honey bee collapse?. Science 327 (2010), 152–153.
49. Rodríguez, M., Vargas, M., Gerding, M., Navarro, H., Antúnez, K., Viral infection and Nosema ceranae in honey bees (Apis mellifera) in Chile. J. Apicul. Res. 51 (2012), 285–287.
50. Rueppell, O., Kaftanouglu, O., Page, R.E., Honey bee (Apis mellifera) workers live longer in small than in large colonies. Exp. Gerontol. 44 (2009), 447–452.
51. Rueppell, O., Hayworth, M.K., Ross, N.P., Altruistic self-removal of health-compromised honey bee workers from their hive. J. Evol. Biol. 23 (2010), 1538–1546.
52. Smart, M.D., Sheppard, W.S., Nosema ceranae in age cohorts of the western honey bee (Apis mellifera). J. Invertebr. Pathol. 109 (2012), 148–151.
53. Smith, M.L., The honey bee parasite Nosema ceranae: transmissible via food exchange?. Plos One, 7(8), 2012, e43319.
54. vanEngelsdorp, D., Evans, J.D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B.K., Frazier, M., Frazier, J., Cox-Foster, D., Chen, Y., Underwood, R., Tarpy, D.R., Pettis, J.S., Colony collapse disorder: a descriptive study. PLoS One, 4, 2009, e6481.
55. vanEngelsdorp, D., Hayes, J. Jr., Underwood, R.M., Caron, D., Pettis, J., A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010. J. Apicult. Res. 50 (2011), 1–10.
56. Vidau, C., Diogon, M., Aufauvre, J., Fontbonne, R., Vigues, B., Brunet, J.L., Texier, C., Biron, D., Blot, N., Alaoui, E., Belzunces, L., Delbac, F., Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS One, 6(6), 2011, e21550.
57. Wang, D.I., Möeller, F.E., The division of labor and queen attendance behavior of Nosema-infected worker honey bees. J. Econ. Entomol. 63 (1970), 1539–1541.
58. Weidner, E., Findley, A.M., Dolgikh, V., Sokolova, J., Microsporidian biochemistry and phisiology. Wittner, M., Weiss, L.M., (eds.) The Microsporidia and Microsporidiosis, 1999, ASM Press, Washington, DC, 172–195.
59. Williams, B.A.P., Unique physiology of host–parasite interactions in microsporidia infections. Cell. Microbiol. 11 (2009), 1551–1560.
60. Williams, G.R., Shutler, D., Rogers, R.E.L., Effects at Nearctic north-temperate latitudes of indoor versus outdoor overwintering on the microsporidium Nosema ceranae and western honey bees (Apis mellifera). J. Invertebr. Pathol. 104 (2010), 4–7.
61. Winston, M.L., The Biology of the Honey Bee. 1987, Harvard University Press, Cambridge, Mass.
62. Wittner, M., Weiss, L.M., The Microsporidia and Microsporidiosis. 1999, ASM Press, Washington, DC.
63. Woyciechowski, M., Kozlowski, J., Division of labor by division of risk according to worker life expectancy in the honey bee (Apis mellifera L.). Apidologie 29 (1998), 191–205.
64. Woyciechowski, M., Moron, D., Life expectancy and onset of foraging in the honeybee (Apis mellifera). Insect. Soc. 56 (2009), 193–201.
65. Xu, W., 2012. A stage-structured model of honeybee population dynamics assessing impacts of pesticides and other stressors. In: Barth, B., Scharpenberg, H., Moritz, R., (Eds.), Proceedings of the Fifth European Conference of Apidology. 3–7th September, Halle an der Saale, Germany. p. 296.