Comparison of the two microsporidia that infect honey bees – a review

Open access

Abstract

Two microsporidian species, Nosema apis and Nosema ceranae, infect honey bees (Apis mellifera) worldwide. They are obligate intracellular parasites that multiply in the epithelial lining of the bee’s midgut and cause nosemosis. N. ceranae infections were primarily found in Apis cerana and raised interest in the last decade with the discovery of their presence in the European honey bee (Apis mellifera). Nosema spp. utilizes hosts’ energetic reserves for the purpose of propagation and disrupts the digestive processes of the bee. Nosemosis reduces the lifespan of a single bee and affects the performance of the colony. It also has an economic impact through the reduction in the honey and pollen yield of severely infected colonies or even causes them to collapse. Lack of effective therapy for nosemosis is of special concern and calls for scientific attention. Although N. ceranae and N. apis are similar in many aspects, there are important differences between them such as clinical signs of infection or the ability to resist low temperatures.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • 1. Adl SM Simpson AGB Farmer MA Andersen RA Anderson OR Barta JR et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 2005; 52: 399-451.

  • 2. Alaux C Folschweiller M McDonnell C Beslay D Cousin M Dussaubat C Brunet JL Le Conte Y. Pathological effects of the microsporidium Nosema ceranae on honey bee queen physiology (Apis mellifera). J. Invertebr. Pathol. 2011; 106: 380-5.

  • 3. Anderson DL Giacon H. Reduced pollen collection by honey bee (Hymenoptera: Apidae) colonies infected with Nosema apis and Sacbrood virus. J. Econ. Entomol. 1992; 85: 47-51.

  • 4. Bailey L. Nosema apis in drone honeybees. J. Apicult. Res. 1972; 11:171-174.

  • 5. Bailey L Ball BV. Microspora and Protozoa. In: Bailey L Ball BV (eds.) Honey bee pathology. Academic Press Limited London UK. 1991:64-77.

  • 6. Botias C Anderson DL Meana A Garrido-Bailon E Martin-Hernandez R Higes M. Further evidence of an oriental origin for Nosema ceranae (Microsporidia: Nosematidae). J. Invertebr. Pathol. 2012; 110:108-13.

  • 7. Botias C Martin-Hernandez 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. http://www.veterinaryresearch.org/content/44/1/25 (21.8.2013)

  • 8. Bourgeois AL Rinderer TE Beaman LD et al. Genetic detection and quantification of Nosema apis and Nosema ceranae in the honey bee. J. Invertebr. Pathol. 2010; 103: 53-58.

  • 9. Cantwell GE. Standard methods for counting Nosema spores. Amer. Bee J. 1970; 110: 222-3.

  • 10. Chaimanee V Warrit N Chantawannakul P. Infections of Nosema ceranae in four different honeybee species. J. Invertebr. Pathol. 2010; 105 2: 207-210.

  • 11. Chaimanee V Chantawannakul P Chen Y Evans JD Pettis JS. Effects of host age on susceptibility to infection and immune gene expression in honey bee queens (Apis mellifera) inoculated with Nosema ceranae. Apidologie 2014; 45(4) 451-463.

  • 12. Copley TR Jabaji SH. 2012. Honeybee glands as possible infection reservoirs of Nosema ceranae and Nosema apis in naturally infected forager bees. J. Appl. Microbiol. 112 15-24.

  • 13. Cornman RS Chen YP Schatz MC et al. Genomic analyses of the Microsporidian Nosema ceranae an emergent pathogen of honey bees. PLOS pathogens 2009; 5: 45-54.

  • 14. Costa C Lodesani M Maistrello L. Effect of thymol and resveratrol administered with candy or syrup on the development of Nosema ceranae and on the longevity of honeybees (Apis mellifera L.) in laboratory conditions. Apidologie 2010; 41 2: 141-150.

  • 15. Czekonska K. The influence of Nosema apis on young honeybee queens and transmission of the disease from queens to workers. Apidologie 2000; 31 6: 701-706.

  • 16. De Grandi-Hoffman G Chen Y Huang E Huang MH. The effect of diet on protein concentration hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.). J. Insect Physiol. 2010; 56: 1184-91.

  • 17. Doull KM. The effects of time of day and method of sampling on the determination of nosema disease in beehives. J. Inverteb. Pathol. 1965; 7: 1-4.

  • 18. Dussaubat C Maisonnasse A Alaux C et al. Nosema spp. infection alters pheromone production in honey bees (Apis mellifera). J. Chem. Ecol. 2010; 36: 522-525.

  • 19. Dussaubat C Brunet JL Higes M Colbourne JK Lopez J Choi JH et al. Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PloS one 2012; 7(5) e37017.

  • 20. Dussaubat C Maisonnasse A Crauser D Beslay D Costagliola G Soubeyrand S et al. Flight behavior and pheromone changes associated to Nosema ceranae infection of honey bee workers (Apis mellifera) in field conditions. J. invertebr. Pathol. 2013; 113: 42-51.

  • 21. Evison SEF Roberts KE Laurenson L Pietravalle S Hui J et al. (2012) Pervasiveness of Parasites in Pollinators. PLoS ONE 7(1): e30641. doi:

    • Crossref
    • Zitation exportieren
  • 22. Forsgren E Fries I. Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet. Parasitol. 2010; 170: 212-217.

  • 23. Fries I. Comb replacement and Nosema disease (Nosema apis) in honey bee colonies. Apidologie 1988; 19: 343-354.

  • 24. Fries I. Observations on the development and transmission of Nosema apis spores Zander in the ventriculus of the honey bee. J. Apicult. Res. 1989; 28: 107-117.

  • 25. Fries I. Infectivity and multiplication of Nosema apis z. in the ventriculus of the honey bee. Apidologie 1988; 19: 319-328.

  • 26. Fries I. Nosema apis - a parasite in the honey bee colony. Bee world 1993; 74 1: 5-19.

  • 27. Fries I. Nosema ceranae in European honey bees (Apis mellifera). J. Invertebr. Pathol. 2010; 103: S73-S79.

  • 28. Fries I Ekbohm G Villumstad E. Nosema apis sampling techniques and honey yield. J. Apicult. Res.1984; 23: 102-105.

  • 29. Fries I Feng F da Silva A Slemenda SB Pieniazek NJ. Nosema ceranae Sp. (Microspora Nosematidae) morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera Apidae). Europ. J. Protistol. 1996; 32: 356-365.

  • 30. Fries I Granados RR Morse RA. Intracellular germination of spores of Nosema apis. Apidologie. 1992; 23: 61-70.

  • 31. Fries I Martin R Meana A Garcia-Palencia P Higes M. Natural infections of Nosema ceranae in European honey bees. J. Apic. Res. 2006; 45: 230-3.

  • 32. Furgala B. The effect of the intensity of Nosema inoculum on queen supersedure in the honey bee Apis mellifera Linnaeus. J. Insect. Pathol. 1962 a; 4: 429-432.

  • 33. Furgala B. Residual fumagillin activity in sugar syrup stored by wintering honeybee colonies. J. Apicult. Res. 1962 b; 1: 35-37.

  • 34. Giersch T Berg T Galea F et al. Nosema ceranae infects honey bees (Apis mellifera) and contaminates honey in Australia. Apidologie 2009; 40: 117-123.

  • 35. Gisder S Hedtke K Moeckel N et al. 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.

  • 36. Gisder S Moeckel N Linde A et al. A cell culture model for Nosema ceranae and Nosema apis allows new insights into the life cycle of these important honey beepathogenic microsporidia. Environ. Microbiol. 2011; 13: 404-413.

  • 37. Gregorc A Fijan N Poklukar J. The effect of Apis mellifera carnica Polm. worker bee source for populating mating nuclei on degree of infection by Nosema apis Zander. Apidologie. 1992; 23: 241-244.

  • 38. Gregorc A. Spremljanje kakovosti vzrejenih matic kranjske čebele za programsko obdobje 2011 - 2013. Report. Agricultural Institute of Slovenia 2013.

  • 39. Hassanein MH. Studies on the effect of infection with Nosema apis on the physiology of the queen honey-bee. J. Cell Sci. 1951; 92: 225-231.

  • 40. Higes M Martin R Meana A. Nosema ceranae a new microsporidian parasite in honeybees in Europe. J. Invertebr. pathol. 2006; 92: 93-95.

  • 41. Higes M Garcia-Palencia P Martin-Hernandez R Meana A. Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J. Invertebr. Pathol. 2007; 94:211-217.

  • 42. Higes M Martin-Hernandez R Botias C Garrido-Bailon E Gonzalez-Porto AV Barrios L del Nozal MJ Bernal JL Jimenez JJ Garcia-Palencia P Meana A. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 2008a; 10: 2659-2669.

  • 43. Higes M Martin-Hernandez R Garrido-Bailon E et al. Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. J. nvertebr. Pathol. 2008b; 97:76-8.

  • 44. Higes M Martin-Hernandez R Garcia-Palencia P et al. Horizontal transmission of Nosema ceranae (Microsporidia) from worker honeybees to queens (Apis mellifera). Environ. Microb. Rep. 2009; 1:495-8.

  • 45. Higes M Martin-Hernandez R Meana A. Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie. 2010; 41:375-92.

  • 46. Higes M Juarranz A Dias-Almeida J Lucena S Botias C Meana A Garcia-Palencia P Martin-Hernandez R. 2013. Apoptosis in the pathogenesis of Nosema ceranae (Microsporidia: Nosematidae) in honey bees (Apis mellifera). Environ. Microbiol. Rep. 5(4) 530-6.

  • 47. Huang WF Jiang JH Chen YW et al. A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 2007; 38: 30-7.

  • 48. Huang WF Solter LF. Comparative development and tissue tropism of Nosema apis and Nosema ceranae. J Invert Pathol 2013; 113 1: 35-41.

  • 49. Klee J Besana AM Genersch E et al. Widespread dispersal of the microsporidian Nosema ceranae an emergent pathogen of the western honey bee Apis mellifera. J. Invertebr. Pathol. 2007; 96 1: 1-10.

  • 50. Kralj J Fuchs S. Nosema sp influences flight behavior of infected honey bee (Apis mellifera) foragers. Apidologie 2010; 41 1: 21-8.

  • 51. Liu TP. Ultrastructure of the midgut of the worker honey bee Apis mellifera heavily infected with Nosema apis. Journal of invertebrate pathology 1984; 44: 282-291.

  • 52. Liu TP. Ultrastructural changes in the secretion granules of the hypopharyngeal glands of the honeybee infected by Nosema apis and after treatment with fumagillin. Tissue and Cell 1990; 22 4: 523-31.

  • 53. Loskotova J Peroutka M Vesely V. Nosema disease of honeybee queens (Apis mellifica). Apidologie 1980; 11 2: 153-61.

  • 54. Maistrello L Lodesani M Costa C Leonardi F Marani G Caldon M Mutinelli F Granato A. Screening of natural compounds for the control of nosema disease in honeybees (Apis mellifera). Apidologie 2008; 39: 436-45.

  • 55. Malone LA Gatehouse HS. 1998. Effects of Nosema apis infection on honey bee (Apis mellifera) digestive proteolytic enzyme activity. J. Invertebr. Pathol. 71 169-74.

  • 56. Martin-Hernandez R Meana A Prieto L Salvador AM Garrido-Bailon E Higes M. 2007. Outcome of colonization of Apis mellifera by Nosema ceranae. Appl. Environ. Microbiol. 73 20: 6331-8.

  • 57. Martin-Hernandez R; Botias C; Barrios L et al. Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitol. Res. 2011; 109 3: 605-12.

  • 58. Mayack C Naug D. Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection J. Invertebr. Pathol. 2009; 100 3: 185-8.

  • 59. Mayack C; Naug D. Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. J. Insect Physiol. 2010; 56 11:1572-5.

  • 60. Matašin Ž Nejedli S Tlak Gajger I. 2012. Leucine aminopeptidase activity in the midgut of nosema diseased honeybees (Apis mellifera). Veterinarski arhiv 82 (6) 599-607.

  • 61. Milbrath MO van Tran T Huang WF Solter LF Tarpy DR Lawrence F Huang ZY. Comparative virulence and competition between Nosema apis and Nosema ceranae in honey bees (Apis mellifera). J. Invertebr Pathol. 2015; 125:9-15. doi:

    • Crossref
    • Zitation exportieren
  • 62. Naug D Gibbs A. Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae. Apidologie 2009; 40 6: 595-9.

  • 63. Paxton RJ Klee J Korpela S et al. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 2007; 38 6: 558-65.

  • 64. Pickard RS Elshemy AAM. Seasonal variation in the infection of honeybee colonies with Nosema apis zander. J. Apicult. Res. 1989; 28 2: 93-100.

  • 65. Plischuk S Martin-Hernandez R Prieto L Lucia M Botias C Meana A Abrahamovich AH Lange C Higes M. South American native bumblebees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia) an emerging pathogen of honeybees (Apis mellifera). Environ. Microb. Rep. 2009; 1 2: 131-135.

  • 66. Porrini MP. Audisio CM. Sabate DC. et al. Effect of bacterial metabolites on microsporidian Nosema ceranae and on its host Apis mellifera. Parasitol. Res. 2010; 107 2: 381-8.

  • 67. Ptaszynska AA Borsuk G Anusiewicz M Mulenko W. Location of Nosema spp. spores within the body of the honey bee. Med. Weter. 2012; 68 10: 618-21.

  • 68. Ptaszyńska A Borsuk G Mułenko W Demetraki-Paleolog J. Differentiation of Nosema apis and Nosema ceranae spores under Scanning Electron Microscopy (SEM) J. Apicult. Res. 2014; 53: 537-544.

  • 69. Sánchez Collado JG Higes M Barrio L Martin-Hernandez R. Flow cytometry analysis of Nosema species to assess spore viability and longevity. Parasitol. Res. 2014; 113 5: 1695-1701.

  • 70. Smith ML. The honey bee parasite Nosema ceranae: transmissible via food exchange? PLoS ONE 2012; 7(8): e43319. doi:

    • Crossref
    • Zitation exportieren
  • 71. Stanimirović Z Stevanović J Bajić V Radović I. Evaluation of genotoxic effects of fumagillin by cytogenetic tests in vivo. Mutation Res. 2007; 628: 1-10.

  • 72. Suwannapong G Maksong S Seanbualuang P Benbow ME. Experimental infection of red dwarf honeybee Apis florea with Nosema ceranae. Journal of Asia-Pacific Entomology 2010; 13: 361-364.

  • 73. Tlak Gajger I Vugrek O Pinter Lj Petrinec Z. “Nozevit patties” treatment of honeybees (Apis mellifera) for the control of Nosema ceranae disease. Am. Bee J. 2009; 149 1053-1056.

  • 74. Tlak Gajger I Vugrek O Grilec D Petrinec Z. Prevalence and distribution of Nosema ceranae in Croatian honeybee colonies. Veterinarni Medicina 2010. 55 9: 457-462.

  • 75. Traver BE Fell RD. Low natural levels of Nosema ceranae in Apis mellifera queens. J. Invertebr. Pathol 2012; 110 3: 408-410.

  • 76. Vavra J Larsson JIR. Structure of the microsporidia. 7 -84. In: Wittner M Weiss LM. 1999. The Microsporidia and microsporidiosis. Washington DC: ASM. 553 p.

  • 77. Vidau C; Diogon M; Aufauvre J et al. Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 2011; 6 6: 56-64.

  • 78. Wang DI Moeller FE. Histological comparisons of the development of hypopharyngeal glands in healthy and nosema-infected worker honey bees. J. Invertebr. Pathol. 1969; 14: 135-42.

  • 79. Wang DI Moeller FE. The division of labor and queen attendance behavior of nosema-infected worker honey bees. J. Econ. Ent. 1970; 63: 1539-41.

  • 80. Wang DI Moeller FE. Ultrastructural changes in hypopharyngeal glands of worker honey bees infected by Nosema apis. J. Invertebr. Pathol. 1971; 17 3: 308-12.

  • 81. Williams GR Sampson MA Shutler D Rogers REL. Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? J. Invertebr. Pathol. 2008; 99 342-4.

  • 82. Wu JY Smart MD Anelli CM Sheppard WS. Honey bees (Apis mellifera) reared in brood combs containing high levels of pesticide residues exhibit increased susceptibility to Nosema (Microsporidia) infection. J. Invertebra. Pathol. 2012; 109 326-9.

Suche
Zeitschrifteninformation
Metriken
Gesamte Zeit Letztes Jahr Letzte 30 Tage
Abstract Views 0 0 0
Full Text Views 482 213 9
PDF Downloads 189 97 5