Parasitology Research

, Volume 109, Issue 3, pp 605–612 | Cite as

Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera)

  • Raquel Martín-Hernández
  • Cristina Botías
  • Laura Barrios
  • Amparo Martínez-Salvador
  • Aránzazu Meana
  • Christopher Mayack
  • Mariano Higes
Original Paper


Nosema ceranae is a relatively new and widespread parasite of the western honeybee Apis mellifera that provokes a new form of nosemosis. In comparison to Nosema apis, which has been infecting the honeybee for much longer, N. ceranae seems to have co-evolved less with this host, causing a more virulent disease. Given that N. apis and N. ceranae are obligate intracellular microsporidian parasites, needing host energy to reproduce, energetic stress may be an important factor contributing to the increased virulence observed. Through feeding experiments on caged bees, we show that both mortality and sugar syrup consumption were higher in N. ceranae-infected bees than in N. apis-infected and control bees. The mortality and sugar syrup consumption are also higher in N. apis-infected bees than in controls, but are less than in N. ceranae-infected bees. With both microsporidia, mortality and sugar syrup consumption increased in function of the increasing spore counts administered for infection. The differences in energetic requirements between both Nosema spp. confirm that their metabolic patterns are not the same, which may depend critically on host–parasite interactions and, ultimately, on host pathology. The repercussions of this increased energetic stress may even explain the changes in host behavior due to starvation, lack of thermoregulatory capacity, or higher rates of trophallaxis, which might enhance transmission and bee death.


  1. Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MFJR (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451PubMedCrossRefGoogle Scholar
  2. Alaux C, Brunet JL, Dussaubat C, Mondet F, Tchamitchan S, Cousin M, Brillard J, Baldy A, Belzunces LP, Le Conte Y (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol 12:774–782PubMedCrossRefGoogle Scholar
  3. Amdam GV, Omholt SW (2003) The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J Theor Biol 223:451–464PubMedCrossRefGoogle Scholar
  4. Antunez K, Martin-Hernandez R, Prieto L, Meana A, Zunino P, Higes M (2009) Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ Microbiol 11:2284–2290PubMedCrossRefGoogle Scholar
  5. Bailey L (1981) Honey bee pathology. Academic Press, LondonGoogle Scholar
  6. Campbell J, Kessler B, Mayack C, Naug D (2010) Behavioral fever in infected honeybees: parasitic manipulation or coincidental benefit? Parasitology 137:1487–1491PubMedCrossRefGoogle Scholar
  7. Chen YP, Evans JD, Murphy C, Gutell R, Zuker M, Gundensen-Rindal D, Pettis JS (2009a) Morphological, molecular and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee Apis mellifera. J Eukaryot Microbiol 56:142–147CrossRefGoogle Scholar
  8. Chen Y, Evans JD, Zhou L, Boncristiani H, Kimura K, Xiao T, Litkowski AM, Pettis JS (2009b) Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J Invertebr Pathol 101:204–209CrossRefGoogle Scholar
  9. De Graaf DC, Raes H, Sabbe G, De Rycke PH, Jacobs FJ (1994) Early development of Nosema apis (Microspora: Nosematidae) in the midgut epithelium of the honeybee (Apis mellifera). J Invertebr Pathol 63:74–81CrossRefGoogle Scholar
  10. Dufort M, Valero Y, Poguet M (1987) Particular distribución de las mitocondrias de Mytilicola intestinalis en células parasitadas por Unikaryon mytilicolae. Rev Iber Parasitol Vol Ext:1–11Google Scholar
  11. Feder D, Mello CB, Garcia ES, Azambuja P (1997) Immune responses in Rhodnius prolixus: influence of nutrition and ecdysone. J Insect Physiol 43:513–519PubMedCrossRefGoogle Scholar
  12. Feigenbaum C, Naug D (2010) The influence of social hunger on food distribution and its implications for disease transmission in a honeybee colony. Insectes Soc 57:217–222CrossRefGoogle Scholar
  13. Fries I, Feng F, da Silva A, Slemenda SB, Pieniazek NJ (1996) Nosema ceranae sp (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur J Protistol 32:356–365Google Scholar
  14. Fries I (2009) Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 103:S73–S79PubMedCrossRefGoogle Scholar
  15. Forsgren E, Fries I (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet Parasitol 170:212–217PubMedCrossRefGoogle Scholar
  16. Gregory PG, Evans JD, Rinderer T, de Guzman L (2005) Conditional immune-gene suppression of honeybees parasitized by Varroa mites. J Insect Sci: 5:7Google Scholar
  17. Harrison JF, Fewell JH (2002) Environmental and genetic influences on flight metabolic rate in the honey bee, Apis mellifera. Comp Biochem Physiol A Mol Integr Physiol 133:323–333PubMedCrossRefGoogle Scholar
  18. Higes M, Martín R, Meana A (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92:93–95PubMedCrossRefGoogle Scholar
  19. Higes M, García-Palencia P, Martín-Hernández R, Meana A (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J Invertebr Pathol 94:211–217PubMedCrossRefGoogle Scholar
  20. Higes M, Martín-Hernández R, Botías C, Bailón EG, González-Porto AV, Barrios L, Nozal MJd, Bernal JL, Jiménez JJ, Palencia PG, Meana A (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10:2659–2669PubMedCrossRefGoogle Scholar
  21. Higes M, Martín-Hernández R, Garrido-Bailón E, González-Porto AV, García-Palencia P, Meana A, Del Nozal MJ, Mayo R, Bernal JL (2009a) Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ Microbiol Reports 1:110–113CrossRefGoogle Scholar
  22. Higes M, Martín-Hernández R, García-Palencia P, Marín P, Meana A (2009b) Horizontal transmission of Nosema ceranae (Microsporidia) from worker honey bees to queens (Apis mellifera). Environ Microbiol Reports 1:495–498CrossRefGoogle Scholar
  23. Higes M, Martín-Hernández R, Meana A (2010) Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41:375–392CrossRefGoogle Scholar
  24. Huang WF, Jiang JH, Chen YW, Wang CH (2007) A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38:30–37CrossRefGoogle Scholar
  25. Howard DF, Tschinkel WR (1980) The effects of colony size and starvation on food flow in the fire ant, Solenopsis invicta (Hymenoptera: Formicidae). Behav Ecol Sociobiol 7:293–300CrossRefGoogle Scholar
  26. Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, Tam DQ, Chinh TX, Puerta F, Ruz JM, Kryger P, Message D, Hatjina F, Korpela S, Fries I, Paxton RJ (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96:1–10PubMedCrossRefGoogle Scholar
  27. Liu TP (1984) Ultrastructure of the midgut of the worker honey bee Apis mellifera heavily infected with Nosema apis. J Invertebr Pathol 44:282–291CrossRefGoogle Scholar
  28. Lloyd S (1995) Environmental influences on host immunity. In: Grenfell T, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, UKGoogle Scholar
  29. Malone LA, Giacon HA, Newton MR (1999) Comparison of the responses of some New Zealand and Australian honey bees (Apis mellifera L) to Nosema apis Z. Apidologie 26:495–502CrossRefGoogle Scholar
  30. Martín-Hernández R, Meana A, Prieto L, Martínez-Salvador A, Garrido-Bailon E, Higes M (2007) Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 73:6331–6338PubMedCrossRefGoogle Scholar
  31. May RM, Anderson RM (1990) Parasite–host coevolution. Parasitology 100:S89–S101PubMedCrossRefGoogle Scholar
  32. Mayack C, Naug D (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol 100:185–188PubMedCrossRefGoogle Scholar
  33. Mayack C, Naug D (2010) Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. J Insect Physiol 56:1572–1575PubMedCrossRefGoogle Scholar
  34. Milinski M (1984) Parasites determine a predator's optimal feeding strategy. Behav Ecol Sociobiol 15:35–37CrossRefGoogle Scholar
  35. Milinski M (1985) Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L) under competition for food. Behaviour 93:203–215CrossRefGoogle Scholar
  36. Moffet JO, Lawson FA (1975) Effect of Nosema-infection on O2 consumption by honey bees. J Econ Entomol 68:627–629Google Scholar
  37. Naug D (2009) Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol Conserv 142:2369–2372CrossRefGoogle Scholar
  38. Naug D, Gibbs A (2009) Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae. Apidologie 40:595–599CrossRefGoogle Scholar
  39. Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol 5:673–677CrossRefGoogle Scholar
  40. Office International des Epizooties (OIE) (2008) Manual of standards for diagnostic test and vaccines [online]. Accessed 20 June 2010
  41. Paxton RJ (2010) Does infection by Nosema ceranae cause "Colony Collapse Disorder" in honey bees (Apis mellifera)? J Apic Res 49:80–84CrossRefGoogle Scholar
  42. Paxton RJ, Klee J, Korpela S, Fries I (2007) Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 38:558–565CrossRefGoogle Scholar
  43. Pulkkinen K, Ebert D (2004) Host starvation decreases parasite load and mean host size in experimental populations. Ecology 85:823–833CrossRefGoogle Scholar
  44. Rinderer TE, Elliot K (1977) Influence of nosematosis on the hoarding behavior of the honeybee. J Invertebr Pathol 30:110–111CrossRefGoogle Scholar
  45. Rothe U, Nachtigall W (1989) Flight of the honey bee. J Comp Physiol B Biochem Syst Environ Physiol 158:739–749CrossRefGoogle Scholar
  46. Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50:529–551PubMedCrossRefGoogle Scholar
  47. Siva-Jothy MT, Thompson JJW (2002) Short-term nutrient deprivation affects immune function. Physiol Entomol 27:206–212CrossRefGoogle Scholar
  48. Sokolova YY, Timoshenko SA, Issi VI (1988) Morphogenesis and ultrastructure of life cycle stages of Nosema mesnili (Microsporidia, Nosematidae). Citologiya 30:26–33Google Scholar
  49. Toth AL, Kantarovich S, Meisel AF, Robinson GE (2005) Nutritional status influences socially regulated foraging ontogeny in honey bees. J Exp Biol 208:4641–4649PubMedCrossRefGoogle Scholar
  50. Yang XL, Cox-Foster DL (2005) Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci USA 102:7470–7475PubMedCrossRefGoogle Scholar
  51. Wakelin D (1989) Nature and nurture: overcoming constraints on immunity. Parasitology 99:S21–S35PubMedCrossRefGoogle Scholar
  52. Walkey M, Meakins RH (1970) An attempt to balance energy budget of a host-parasite system. J Fish Biol 2:361–372CrossRefGoogle Scholar
  53. Weidner E, Findley AM, Dolgidh V, Sokolova J (1999) Microsporidian biochemistry and physiology. In: Wittner M, Weiss LM (eds) The microsporidia and microsporidiosis. ASM Press, Washington, DC, pp 172–195Google Scholar
  54. Williams BAP (2009) Unique physiology of host-parasite interactions in microsporidia infections. Cell Microbiol 11:1551–1560PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Raquel Martín-Hernández
    • 1
  • Cristina Botías
    • 1
  • Laura Barrios
    • 2
  • Amparo Martínez-Salvador
    • 3
  • Aránzazu Meana
    • 4
  • Christopher Mayack
    • 5
  • Mariano Higes
    • 1
  1. 1.Bee Pathology LaboratoryCentro Apícola Regional, JCCMMarchamaloSpain
  2. 2.Statistics Department, CTIConsejo Superior Investigaciones CientíficasMadridSpain
  3. 3.Epidemiology DepartmentTRAGSEGAMadridSpain
  4. 4.Animal Health Department, Facultad de VeterinariaUniversidad Complutense de MadridMadridSpain
  5. 5.Department of BiologyColorado State UniversityFort CollinsUSA

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