Effects of Nosema ceranae and thiametoxam in Apis mellifera: A comparative study in Africanized and Carniolan honey bees

Chemosphere

Volumn 147, Issue , 2016, Pages 328-336

  Gregorc, Ales ^a   Silva Zacarin, Elaine C M ^b   Carvalho, Stephan Malfitano ^c   Kramberger, Doris ^d   Teixeira, Erica W ^e   Malaspina, Osmar ^f  

^a AGRICULTURAL INSTITUTE OF SLOVENIA   (Slovenia)

^b FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^c FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

^d UNIVERSITY OF MARIBOR   (Slovenia)

^e AGÊNCIA PAULISTA DE TECNOLOGIA DOS AGRONEGÓCIOS   (Brazil)

^f SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Cell death; Midgut; Neonicotinoid; Pathogen; Worker honey bee

Indexed keywords

CELL DEATH; PATHOGENS;

APIS MELLIFERA; COMPARATIVE STUDIES; EXPERIMENTAL CONDITIONS; FIELD CONDITIONS; HONEY BEE; MIDGUT; MULTIPLE STRESSORS; NEONICOTINOIDS;

FOOD PRODUCTS;

NEONICOTINOID; THIAMETHOXAM; INSECTICIDE; NITRO DERIVATIVE; OXAZINE DERIVATIVE; THIAZOLE DERIVATIVE;

COMPARATIVE STUDY; FUNGUS; HONEYBEE; PATHOGEN; THIAMETHOXAM; TOXICITY TEST;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APIS MELLIFERA; ARTICLE; CELL DEATH; CONTROLLED STUDY; FUNGUS SPORE; IMMUNOHISTOLOGY; LD50; MIDGUT; NONHUMAN; NOSEMA CERANAE; ANIMAL; BEE; CHEMISTRY; DRUG EFFECTS; GENETICS; LONGEVITY; MICROBIOLOGY; NOSEMA;

APIS MELLIFERA; APOIDEA; NOSEMA; NOSEMA CERANAE;

ANIMALS; BEES; INSECTICIDES; LONGEVITY; NITRO COMPOUNDS; NOSEMA; OXAZINES; SPORES, FUNGAL; THIAZOLES;

EID: 84957799809     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2015.12.030     Document Type: Article

References (37)

1. Alaux C., Brunet J.L., 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.
2. Aufauvre J., Biron D.G., Vidau C., Fontbonne R., Roudel M., Diogon M., Vigues B., Belzunces L.P., Delbac F., Blot N. Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee. Sci. Rep. 2012, 2:326.
3. Aufauvre J., Misme-Aucouturier B., Vigues B., Texier C., Delbac F., Blot N. Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLos One 2014, 9:e91686.
4. Bernet D., Schmidt H., Meier W., Burkhardt-Holm P., Wahli T. Histopathology in fish: proposal for a protocol to assess aquatic pollution. J. Fish. Dis. 1999, 22:25-34.
5. Botías C., Martín-Hernández R., Barrios L., Meana A., Higes M. Nosema spp: Infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet. Res. 2013, 44:25.
6. Calderón R.A., Van Veen J.W., Sommeijer M.J., Sanchez L.A. Reproductive biology of Varroa destructor in Africanized honey bees (Apis mellifera). Exp. Appl. Acarol. 2010, 50:281-297.
7. Cornman R.S., Tarpy D.R., Chen Y., Jeffreys L., Lopez D., Pettis J.S., Van Engelsdorp D., Evans J.D. Pathogen Webs in collapsing honey Bee colonies. PLos One 2012, 7:e43562.
8. Cox-Foster D.L., Conlan S., Holmes E.C., Palacios G., Evans J.D., Moran N.A. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 2007, 318:283-287.
9. Decourtye A., Devillers J., Genecque E., Le Menach K., Budzinski H., Cluzeau S., Pham-Delegue M.H. Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch. Environ. Contam. Toxicol. 2005, 48:242-250.
10. Del Aguila C., Izquierdo F., Granja A.G., Hurtado C., Fenoy S., Fresno M., Revilla Y. Encephalitozoon microsporidia modulates p53-mediated apoptosis in infected cells. Int. J. Parasitol. 2006, 36:869-876.
11. Dussaubat C., Brunet J.L., Higes M., Colbourne J.K., López J., Choi J.H. Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS One 2012, 7:e37017.
12. Dussaubat C., Maisonnasse A., Alaux C., Tchamitchan S., Brunet J.L., Plettener E. Nosema spp. infectation alters pheromone production in honey bee (Apis mellifera). J. Chem. Ecol. 2010, 36:522-525.
13. García-Palencia P., Martín-Hernández R., González-Porto A.V., Marin P., Meana A., Higes M. Natural infection by Nosema ceranae causes similar lesions as in experimentally infected caged-worker honey bees (Apis mellifera). J. Apic. Res. 2010, 49:278-283.
14. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 1992, 119:493-501.
15. Girolami V., Mazzon L., Squartini A., Mori N., Marzaro M., Di Bernardo A., Greatti M., Giorio C., Tapparo A. Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: a novel way of intoxication for bees. J. Econ. Entomol. 2009, 102:1808-1815.
16. Godfray H.C.J., Blacquièren T., Field L.M., Hails R.S., Petrokofsky G., Potts S.G., Raine N.E., Vanbergen A.J., McLean A.R. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. R. Soc. B 2014, 281:20140558.
17. Goulson D., Nicholls E., Botías C., Rotheray E.L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 2015, 347. 10.1126/science.1255957.
18. Guzmán-Novoa E., Vandame R., Arechavaleta M.E. Susceptibility of European and Africanized honey bees (Apis mellifera L.) to Varroa jacobsoni Oud. in Mexico. Apidologie 1999, 30:173-182.
19. Gregorc A., Bowen I.D. Histochemical characterization of cell death in honeybee larvae midgut after treatment with Paenibacillus larvae, amitraz and oxytetracycline. Cell Biol. Int. 2000, 24:319-324.
20. Higes M., Garcia-Palencia P., Martín-Hernández R., Meana A. Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J. Invertebr. Pathol. 2007, 94:211-217.
21. Higes M., Martín-Hernández R., Botías C., Garrido-Bailón E., González-Porto A.V., Barrios L. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 2008, 10:2659-2669.
22. Huang W.F., Solter L.F. Comparative development and tissue tropism of Nosema apis and Nosema ceranae. J. Invertebr. Pathol. 2013, 113:35-41.
23. James E.R., Green D.R. Infection and the origins of apoptosis. Cell Death Differ. 2002, 9:355-357.
24. Maienfisch P., Angst M., Brandl F., Fischer W., Hofer D., Kayser H., Kobel W., Rindlisbacher A., Senn R., Steinemann A., Widmer H. Chemistry and biology of thiamethoxam: a second generation neonicotinoid. Pest Manag. Sci. 2001, 57:906-913.
25. Martín-Hernández R., Meana A., Prieto L., Salvador A.M., Garrido-Bailon E. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol. 2007, 73:6331-6338.
26. Matylevitch N.P., Schuschereba S.T., Mata J.R., Gilligan G.R., Lawlor D.F., Goodwin C.W., Bowman P.D. Apoptosis and accidental cell death in cultured human keratinocytes after thermal injury. Am. J. Pathol. 1998, 153:567-577.
27. Oliveira R.A., Roat T.C., Carvalho S.M., Malaspina O. Side-effects of thiamethoxam on the brain and midgut of the africanized honeybee (Hymenopptera: Apidae). Environ. Toxicol. 2014, 29:1122-1133.
28. Pilling E., Campbell P., Coulson M., Ruddle N., Tornier I. A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam. PLoS One 2013, 8. 10.1371/journal.pone.0077193.
29. Pettis J.S., Van Engelsdorp D., Johnson J., Dively G. Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 2012, 99:153-158.
30. 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, 118C:18-19.
31. Sandrock C., Tanadini M., Tanadini L.G., Fauser-Misslin A., Potts S.G. Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure. PLoS One 2014, 9:e103592.
32. Scanlon M., Leitch G.J., Shaw A.P., Moura H., Visvesvara G.S. Susceptibility to apoptosis is reduced in the microsporidia infected host. J. Eukaryot. Microbiol. 1999, 46:34S-35S.
33. Stoner K.A., Eitzer B.D. Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS One 2012, 7:e39114.
34. Teixeira E.W., Santos L.G., Sattler A., Message D., Alves M.L.T.M.F., Martins M.F., Grassi-Sell M.L., Francoy T.M. Nosema ceranae has been present in Brazil for more than three decades infecting Africanized honey bees. J. Invertebr. Pathol. 2013, 114:250-254.
35. Tan J., Galligan J.J., Hollingworth R.M. Agonist actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. Neurotoxicol 2007, 28:829-842.
36. Van Engelsdorp 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 2009, 4:e6481.
37. Vidau C., Diogon M., Aufauvre J., Fontbonne R., Vigues B. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS One 2011, 6:e21550.