Characterizing the impact of commercial pollen substitute diets on the level of Nosema spp. in Honey Bees (Apis mellifera L.)

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Fleming, James C ^a   Schmehl, Daniel R ^a,b   Ellis, James D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b BAYER CROPSCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; APIS MELLIFERA; ARTICLE; COMMERCIAL DIET; CONTROLLED STUDY; DIET SUPPLEMENTATION; HOST PATHOGEN INTERACTION; INOCULATION; LIMIT OF QUANTITATION; MIDGUT; NONHUMAN; NOSEMA; ORGANISM COLONY; POLLEN; ANIMAL; BEE; DIET; DIETARY SUPPLEMENT; FUNGUS SPORE; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; UTILIZATION;

ANIMALS; BEES; DIET; DIETARY SUPPLEMENTS; NOSEMA; POLLEN; SPORES, FUNGAL;

EID: 84941964383     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132014     Document Type: Article

References (44)

1. Gisder S, Möckel N, Linde A, Genersch E (2011) A cell culture model for Nosema ceranae and Nosema apis allows new insights into the life cycle of these important honey bee-pathogenic microsporidia. Environ Microbiol 13: 404-413. doi: 10.1111/j.1462-2920.2010.02346.x PMID: 20880328
2. Eilers EJ, Kremen C, Greenleaf SS, Garber AK, Klein A-M (2011) Contribution of pollinator-mediated crops to nutrients in the human food supply. PLoS ONE 6: e21363. doi: 10.1371/journal.pone.0021363 PMID: 21731717
3. Morse RA, CalderoneNW (2000) The value of honey bees as pollinators of US crops in 2000. Bee Culture 128: 1-15.
4. van Engelsdorp D, Caron D, Hayes J, Underwood R, Henson M, Rennich K, et al. (2012) A national survey of managed honey bee 2010-11 winter colony losses in the USA: results from the Bee Informed Partnership. J Apicult Res 51: 115-124.
5. Ciarlo TJ, Mullin CA, Frazier JL, Schmehl DR (2012) Learning impairment in honey bees caused by agricultural spray adjuvants. PLoS ONE 7: e40848. doi: 10.1371/journal.pone.0040848 PMID: 22815841
6. Collins AM, Pettis JS, Wilbanks R, Feldlaufer MF (2004) Performance of honey bee (Apis mellifera) queens reared in beeswax cells impregnated with coumaphos. J Apicult Res 43: 128-134.
7. Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delègue M-H (2004) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotox Environ Safe 57: 410-419.
8. Decourtye A, Devillers J, Genecque E, Le Menach K, Budzinski H, Cluzeau S, et al. (2005) Comparative sublethal toxicity of nine pesticides on olfactory learning performances of the honeybee Apis mellifera. Arch Environ Con Tox 48: 242-250.
9. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52: 81-106. PMID: 16842032
10. Eiri DM, Nieh JC (2012) A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. J Exp Biol 215: 2022-2029. doi: 10.1242/jeb.068718 PMID: 22623190
11. Frost EH, Shutler D, Hillier NK (2013) Effects of fluvalinate on honey bee learning, memory, responsiveness to sucrose, and survival. J Exp Biol 216: 2931-2938. doi: 10.1242/jeb.086538 PMID: 23619403
12. Haarmann T, Spivak M, Weaver D, Weaver B, Glenn T (2002) Effects of fluvalinate and coumaphos on queen honey bees (Hymenoptera: Apidae) in two commercial queen rearing operations. J Econ Entomol 95: 28-35. PMID: 11942761
13. Henry M, Beguin M, Requier F, Rollin O, Odoux J-F, Aupinel P,et al. (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336: 348-350. doi: 10.1126/science.1215039 PMID: 22461498
14. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, Pettis J (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5: e9754. doi: 10.1371/journal.pone.0009754 PMID: 20333298
15. Oldroyd BP (2007) What's killing American honey bees? PLoS Biol 5: e168. PMID: 17564497
16. Williamson SM, Wright GA (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 216: 1799-1807. doi: 10.1242/jeb.083931 PMID: 23393272
17. Zhu W, Schmehl DR, Mullin CA, Frazier JL (2014) Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLoS ONE 9: e77547. doi: 10.1371/journal.pone.0077547 PMID: 24416121
18. Brodschneider R, Crailsheim K (2010) Nutrition and health in honey bees. Apidologie 41: 278-294.
19. Hrassnigg N, Crailsheim K (2005) Differences in drone and worker physiology in honeybees (Apis mellifera). Apidologie 36: 255-277.
20. Naug D, Gibbs A (2009) Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae. Apidologie 40: 595-599.
21. Crailsheim K, Schneider LHW, Hrassnigg N, Bühlmann G, Brosch U, Gmeinbauer R, et al. (1992) Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): Dependence on individual age and function. J Insect Physiol 38: 409-419.
22. Mattila HR, Otis GW (2006) Influence of Pollen Diet in Spring on Development of Honey Bee (Hymenoptera: Apidae) Colonies. J Econ Entomol 99: 604-613. PMID: 16813288
23. DeGrandi-Hoffman G, Chen Y, Huang E, Huang MH (2010) The effect of diet on protein concentration, hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.). J Insect physiol 56: 1184-1191. doi: 10.1016/j.jinsphys.2010.03.017 PMID: 20346950
24. Naug D (2009) Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol Conserv 142: 2369-2372.
25. Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222: 187-209.
26. Standifer LN, Moeller FE, Kauffeld NM, Herbert EW, Shimanuki H (1977) Supplemental feeding of honey bee colonies. USDA Agr Inform Bull 413, 8p.
27. Wahl O, Ulm K (1983) Influence of pollen feeding and physiological condition on pesticide sensitivity of the honey bee Apis mellifera carnica. Oecologia 59: 106-128. doi: 10.1007/BF00388082 PMID: 25024157
28. Aliouane Y, el Hassani AK, Gary V, Armengaud C, Lambin M, Gauthier M (2009) Subchronic exposure of honeybees to sublethal doses of pesticides: Effects on behavior. Environ Toxicol and Chem 28: 113-122.
29. Schmehl DR, Teal PEA, Frazier JL, Grozinger CM (2014) Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera). J Insect Physiol 71: 177-190. doi: 10.1016/j.jinsphys.2014.10.002 PMID: 25450567
30. Ewald PW (1983) Host-parasite relations, vectors, and the evolution of disease severity. Annu Rev Ecol Syst 465-485.
31. Forsgren E, Fries I (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet Parasitol 170: 212-217. doi: 10.1016/j.vetpar.2010.02.010 PMID: 20299152
32. Cantwell G (1970) Standard methods for counting Nosema spores. Am Bee J 110: 22-223.
33. Matheson A (1996) World bee health update. Bee World 77: 45-51.
34. Zander E (1909) Tierische Parasiten als Krankheitserreger bei der Biene, Münchener Bienenzeitung 31, 196-204.
35. Bigliardi E, Sacchi L (2001) Cell biology and invasion of the microsporidia. Microbes Infect 3: 373-379. PMID: 11369274
36. Pickard R, El-Shemy A (1989) Seasonal variation in the infection of honeybee colonies with Nosema apis Zander. J Apicult Res 28: 93-100.
37. Malone LA, Gatehouse HS (1998) Effects of Nosema apis Infection on Honey Bee (Apis mellifera) Digestive Proteolytic Enzyme Activity. J Invertebr Pathol 71: 169-174.
38. Fries I, Chauzat M-P, Chen Y-P, Doublet V, Genersch E, Gisder S, et al. (2013) Standard methods for Nosema research. J Apicult Res 52: 1-14.
39. Porrini MP, Sarlo EG, Medici SK, Garrido PM, Porrini DP, Damiani N,et al. (2011) Nosema ceranae development in Apis mellifera: influence of diet and infective inoculum. J Apicult Res 50: 35-41.
40. Williams GR, Alaux C, Costa C, Csáki T, Doublet V, Eisenhardt D, et al. (2013) Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. J Apicult Res 52: 1-35.
41. Vojvodic S, Rehan SM, Anderson KE (2013) Microbial Gut diversity of Africanized and European honey Bee larval instars. PLoS ONE 8: e72106. doi: 10.1371/journal.pone.0072106 PMID: 23991051
42. Olsen PE, Rice WA, Liu TP (1986) In vitro germination of Nosema apis spores under conditions favorable for the generation and maintenance of sporoplasms. J Invertebr Pathol 47: 65-73.
43. Haydak M (1935) Brood rearing by honeybees confined to a pure carbohydrate diet. J Econ Entomol 28: 657-660.
44. Rinderer TE, Dell Elliott K (1977) Worker honey bee response to infection with Nosema apis: influence of diet. J Econ Entomol 70: 431-433.