Comparative virulence and competition between Nosema apis and Nosema ceranae in honey bees (Apis mellifera)

Journal of Invertebrate Pathology

Volumn 125, Issue , 2015, Pages 9-15

  Milbrath, Meghan O ^a   van Tran, Toan ^a,b   Huang, Wei Fong ^c   Solter, Leellen F ^c   Tarpy, David R ^d   Lawrence, Frank ^a   Huang, Zachary Y ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Bee Research and Development Centre   (Viet Nam)

^c UNIVERSITY OF ILLINOIS   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Co infection, mixed infections; Disease transmission, infectivity; Honey bee, apis mellifera; Microsporidia; Microsporidiosis; Nosema apis; Nosema ceranae

Indexed keywords

APIS MELLIFERA; APOIDEA; MICROSPORIDIA; NOSEMA; NOSEMA APIS; NOSEMA CERANAE;

ANIMAL; BACTERIAL COUNT; BEE; COMPARATIVE STUDY; HOST PATHOGEN INTERACTION; MICROBIOLOGY; NOSEMA; PHYSIOLOGY; SPECIES DIFFERENCE;

ANIMALS; BEES; COLONY COUNT, MICROBIAL; HOST-PATHOGEN INTERACTIONS; NOSEMA; SPECIES SPECIFICITY;

EID: 84920972482     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2014.12.006     Document Type: Article

References (35)

1. Allen J., Le H. An additional measure of overall effect size for logistic regression models. J. Educ. Behav. Stat. 2008, 33:416-441.
2. Bourgeois L., Beaman L., Holloway B., Rinderer T. External and internal detection of Nosema ceranae on honey bees using real-time PCR. J. Invertebr. Pathol. 2012, 109:232-235.
3. Bourgeois A.L., Rinderer T.E., Sylvester H.A., Holloway B., Oldroyd B.P. Patterns of Apis mellifera infestation by Nosema ceranae support the parasite hypothesis for the evolution of extreme polyandry in eusocial insects. Apidologie 2012, 43:539-548.
4. 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. 2008, 97:186-188.
5. Chen Y., Evans J.D., Zhou L., Boncristiani H., Kimura K., Xiao T., Litkowski A.M., Pettis J.S. Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J. Invertebr. Pathol. 2009, 101:204-209.
6. Chen Y.P., Evans J.D., Murphy C., Gutell R., Zuker M., Gundensen-Rindal D., et al. Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. J. Eukaryotic Microbiol. 2009, 56:142-147.
7. Chen Y.-W., Chung W.-P., Wang C.-H., Solter L.F., Huang W.-F. Nosema ceranae infection intensity highly correlates with temperature. J. Invertebr. Pathol. 2012, 111:264-267.
8. Cohen J. A power primer. Psychol. Bull. 1992, 112:155-159.
9. Copley T.R., Chen H., Giovenazzo P., Houle E., Jabaji S.H. Prevalence and seasonality of Nosema species in Québec honey bees. Can. Entomol. 2012, 144:577-588.
10. Cox D., Snell E.J. The Analysis of Binary data 1989, Chapman & Hall.
11. Fenoy S., Rueda C., Higes M., Martín-Hernández R., del Aguila C. High-level resistance of Nosema ceranae, a parasite of the honeybee, to temperature and desiccation. Appl. Environ. Microb. 2009, 75:6886-6889.
12. Forsgren E., Fries I. Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet. Parasitol. 2010, 170:212-217.
13. Fries I. Nosema ceranae in European honey bees (Apis mellifera). J. Invertebr. Pathol. 2010, 103. S73-9.
14. Fries I., Feng F., da Silva 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. Protistol. 1996, 32:356-365.
15. Gisder S., Hedtke K., Möckel N., Frielitz M.-C., Linde A., Genersch E. Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae?. Appl. Environ. Microbiol. 2010, 76:3032-3038.
16. Higes M., García-Palencia P., Martín-Hernández R., Meana A. Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J. Invertebr. Pathol. 2007, 94:211-217.
17. Higes M., Martín-Hernández R., Garrido-Bailón E., García-Palencia P., Meana A. Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. J. Invertebr. Pathol. 2008, 97:76-78.
18. Higes M., Meana A., Bartolomé C., Botías C., Martín-Hernández R. Nosema ceranae (Microsporida), a controversial 21st century honey bee pathogen. Environ. Microbiol. Rep. 2013, 5:17-29.
19. Hoch G., D'Amico V., Solter L.F., Zubrik M., McManus M.L. Quantifying horizontal transmission of Nosema lymantriae, a microsporidian pathogen of the gypsy moth, Lymantria dispar (Lep., Lymantriidae) in field cage studies. J. Invertebr. Pathol. 2008, 99:146-150.
20. Huang W.-F., Solter L.F. Comparative development and tissue tropism in Nosema apis and Nosema ceranae. J. Invertebr. Pathol. 2013, 113:35-41.
21. Huang W.-F., Jiang J.-H., Chen Y.-W., Wang C.-H. A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 2007, 38:30-37.
22. Huang W.-F., Solter L.F., Yau P.M., Imai B.S. Nosema ceranae escapes Fumagillin control in honey bees. PLoS Pathogens 2013, 9:e1003185.
23. 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. 2007, 96:1-10.
24. Martín-Hernández R., Botías C., Bailón E.G., Martínez-Salvador A., Prieto L., Meana A., Higes M. Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis?. Environ. Microbiol. 2012, 14:2127-2138.
25. Milbrath M.O., Xie X., Huang Z.Y. Nosema ceranae induced mortality in honey bees (Apis mellifera) depends on infection methods. J. Invertebr. Pathol. 2013, 114:42-44.
26. Murphy K., Myors B. Statistical Power Analysis: A Simple and General Model for Traditional and Modern Hypothesis Tests 2003, Routledge, New York. second Ed.
27. Paxton R.J., Klee J., Korpela S., Fries I. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 2007, 38:558-565.
28. Peng C.-Y.J., Lee K.L., Ingersoll G.M. An introduction to logistic regression analysis and reporting. J. Educ. Res. 2002, 96:3-14.
29. Pilarska D.K., Solter L.F., Kereselidze M., Linde A., Hoch G. Microsporidian infections in Lymantria dispar larvae: interactions and effects of multiple species infections on pathogen horizontal transmission. J. Invertebr. Pathol. 2006, 93:105-113.
30. R Development Core Team, 2010. R: A Language and Environment for Statistical Computing.
31. Smithson M., Verkuilen J. A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychol. Methods 2006, 11:54-71.
32. Solter L.F., Becnel J.J., Vavra J. Research methods for entomopathogenic microsporidia and other protists. Manual of Techniques in Invertebrate Pathology 2012, 329-371. Elsevier, San Diego. L.A. Lacey (Ed.).
33. Solter L.F., Siegel J.P., Pilarska D.K., Higgs M.C. The impact of mixed infection of three species of microsporidia isolated from the gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae). J. Invertebr. Pathol. 2002, 81:103-113.
34. Walsh P.S., Metzger D.A., Higuchi R. Chelex® 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 1991, 10:506-513.
35. Zander E. Tierische parasiten als krankheitserreger bei der biene. Munchener Bienenzeitung 1909, 31:196-204.