, Volume 49, Issue 6, pp 781–788 | Cite as

Onset of foraging and lifespan of Africanized honey bees (Apis mellifera) infected with different levels of Nosema ceranae spores in Neotropical Mexico

  • Fernando A. Fleites-Ayil
  • José Javier G. Quezada-Euán
  • Luis A. Medina-MedinaEmail author
Original article


Nosema ceranae is a microsporidium pathogen widely spread around the world. Negative effects on foraging behavior and longevity of EHB colonies have been associated with this pathogen as well as possible population losses, but its effects have not been studied in tropical adapted honey bees. We studied the interaction between this pathogen and Africanized honey bees (AHB) in the Yucatan peninsula of Mexico where N. ceranae has only been detected since 2008. Non-infected and artificially infected workers with two different spore concentrations were introduced in observation hives to evaluate the onset and duration of foraging and longevity. The results showed precocious foraging, a reduction of the duration of foraging and a decrease in the longevity of infected bees compared with non-infected ones. However, the results indicate that although negative effects can be caused by N. ceranae in AHB, these were of a moderate magnitude compared with similar reports on EHB in temperate areas. Further research is necessary to evaluate the long-term effect of N. ceranae on AHBs in relation to colony dynamics to better understand the absence of significant colony losses associated with this pathogen in tropical and subtropical Mexico.


Nosema ceranae foraging behavior longevity Nosemosis Africanized bees 



We thank Dr. Robert Paxton and PhD candidate Alice Séguret for constructive discussions and revision of the manuscript. We also thank Dr. Fernando Puerto Manzano for assistance in the molecular evaluations and Manuel Vazquez and Omar Sosa for assistance in laboratory and field observations.

Authors’ contributions

All authors have contributed equally to the work.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Antúnez, K., Martín-Hernández, 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 (9), 2284–2290CrossRefPubMedGoogle Scholar
  2. Botías, C., Martín-Hernández, R., Barrios, L., Meana, A., Higes, M. (2013) Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet. Res. 44, 25CrossRefPubMedPubMedCentralGoogle Scholar
  3. Cantwell, G.E. (1970) Standard methods for counting nosema spores. American Bee Journal 110 (6), 222–223Google Scholar
  4. Chen, Y., Evans, J.D., Smith, I.B., Pettis, J.S. (2008) 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. 97, 186–188CrossRefPubMedGoogle Scholar
  5. Domínguez-Ayala, R., Moo-Valle, H., May-Itzá, W. de J., Medina-Peralta, S., Quezada-Euán, J. J. G. (2016) Stock composition of northern neotropical honey bees: mitotype and morphotype diversity in Mexico (Hymenoptera: Apidae). Apidologie 47, 642–652CrossRefGoogle Scholar
  6. Dussaubat, C., Maisonnasse, A., Crauser, D., Beslay, D., Costagliola, G., Soubeyrand, S., Kretzchmar, A., Le Conte, Y. (2013) Flight behavior and pheromone changes associated to Nosema ceranae infection of honeybee workers (Apis mellifera) in field conditions. J Invertebr Pathol. 113:42–51CrossRefPubMedGoogle Scholar
  7. Fries, I., Ekbohm, G., Villumstad, E. (1984) Nosema apis, sampling techniques and honey yield. J. Apic. Res. 23(2), 102–105CrossRefGoogle Scholar
  8. Fries, I., Chauzat, M.P., Chen, Y.P., Doublet, V., Genersch, E., et al. (2013) Standard methods for Nosema research. J. Apic. Res. 52 (1), 1–28CrossRefGoogle Scholar
  9. García-Millán, M., Quezada-Euán, J.J. (1993) Distribución de la Nosemosis en apiarios comerciales del estado de Yucatán. Apicultura Moderna 5, 22–24Google Scholar
  10. Garnery, L., Solignac, M., Celebrano, G., Cornuet, J.M., (1993) A simple test using restricted PCR-amplified mitochondrial DNA to study the genetic structure of Apis mellifera L. Experientia 49, 1016–1020CrossRefGoogle Scholar
  11. Goblirsch, M., Huang, Z.Y., Spivak, M. (2013) Physiological and behavioral changes in honey bees (Apis mellifera) induced by Nosema ceranae infection. Plos One. 8 (3), 1–8CrossRefGoogle Scholar
  12. Goulson, D., Nicholls, E., Botías, C., Rotheray, E. (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. 347, 1–7CrossRefGoogle Scholar
  13. Gregorc, A., Silva-Zacarin, E., Malfitano, S., Kramberger, D., Teixeira, E., Malaspina, O. (2016) Effects of Nosema ceranae and thiametoxam in Apis nellifera: A comparative study in Africanized and Carniolan Honey bees. Chemosphere. 147, 328–336CrossRefPubMedGoogle Scholar
  14. Guerrero-Molina, C., Correa-Benítez, A., Hamiduzzaman, M.M., Guzman-Novoa, E. (2016) Nosema ceranae is an old resident of honey bee (Apis mellifera) colonies in Mexico, causing infection levels of one million spores per bee or higher during summer and fall. J. Invertebr. Pathol. 141, 38–40CrossRefPubMedGoogle Scholar
  15. Guzmán-Novoa, E., Hamiduzzaman, M.M., Arechavaleta, M.E., Koleoglu, G. (2011) Nosema ceranae has parasited Africanized honey bees in Mexico since at least 2004. J. Apicul. Res. 50 (2), 167–169CrossRefGoogle Scholar
  16. Hart, A.G., Ratnieks, F.L.W. (2001) Why do honey-bee (Apis mellifera) foragers transfer nectar to several receivers? Information improvement through multiple sampling in a biological system. Behav. Ecol. Sociobiol. 49, 244–250CrossRefGoogle Scholar
  17. Higes, M., Martín-Hernández, R., Meana, A. (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J. Invertebr. Pathol. 92, 93–95CrossRefPubMedGoogle Scholar
  18. 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, 211–217CrossRefPubMedGoogle Scholar
  19. Higes, M., Martín-Hernández, R., Botías, C., Garrido-Bailón, E., González-Porto, A.V. et al. (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 10 (10), 2659–2669CrossRefPubMedGoogle Scholar
  20. Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A.V., García-Palencia, P., Meana, A., Del Nozal, M.J., Mayo, R., Bernal, J.L. (2009) Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environ. Microbiol. Rep. 1, 110–113Google Scholar
  21. Holt, H.L., Aronstein, K.A., Grozinger, C.M. (2013) Chronic parasitization by Nosema microsporidia causes global expression changes in core nutritional, metabolic and behavioral pathways in honey bee workers (Apis mellifera). BMC Genom. 14, 1–16CrossRefGoogle Scholar
  22. Human, H., Brodschneider, R., Dietemann, V., Dively, G., Ellis, J. et al. (2013) Miscellaneous standard methods for Apis mellifera research. J. Apicul. Res. 52 (4), 1–56CrossRefGoogle Scholar
  23. Kolmes, S.A. (1984) A quantitative comparison of behavior methodologies for studies of worker honeybees. J. Apicul. Res. 23 (4): 189–198CrossRefGoogle Scholar
  24. Kralj, J., Fuchs, S. (2010) Nosema spp. influences flight behavior of infected honey bee (Apis mellifera) foragers. Apidologie 41: 21–28CrossRefGoogle Scholar
  25. Lecocq, A., Jensen, A., Kryger. P., Nieh, J. (2016) Parasite infection accelerates age polyethism in Young honey bees. Sci. Rep., DOI:
  26. Mayack, C.; Naug, D. (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J. Invertebr. Pathol. 100, 185–88CrossRefPubMedGoogle Scholar
  27. McMahon, D.P., Natsopoulou, M.E., Doublet, V., Fürst, M., Weging, S., Brown, M.J.F., Gogol-Döring, A., Paxton, R.J. (2016) Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc. R. Soc. B 283, 20160811CrossRefPubMedGoogle Scholar
  28. Martínez-Puc, J.F., Medina-Medina, L.A., Catzin-Ventura, G. (2011) Frecuencia de Varroa destructor, Nosema apis y Acarapis woodi en colonias manejadas y enjambres silvestres de abejas (Apis mellifera) en Mérida, Yucatán, México. Rev. Mex. Cien. Pecu. 2 (1), 25–38Google Scholar
  29. Natsopoulou, M.E., McMahon, D.P., Paxton, R.J. (2016) Parasites modulate within-colony activity and accelerate the temporal polyethism schedule of a social insect, the honey bee. Behav Ecol Sociobiol.70 (7), 1019–1031CrossRefPubMedGoogle Scholar
  30. Naug, D. (2014) Infected honeybee foragers incur a higher loss in efficiency than in the rate of energetic gain. Biol. Lett. 10, 20140731CrossRefPubMedPubMedCentralGoogle Scholar
  31. Nielsen D.I., Ebert, P.R., Hunt, G.R., Guzmán-Novoa, E., Kinnee, S.A., Page, R.E. (1999) Identification of Africanized honey bees (Hymenoptera: Apidae) incorporating morphometrics and an improved polymerase chain reaction mitotyping procedure. A. Entom. Soc. Ame. 92 (2), 167–174CrossRefGoogle Scholar
  32. Paxton, R., 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 (6), 558–565CrossRefGoogle Scholar
  33. Quezada-Euán, J.J.G. (2007) A retrospective history of the expansion of Africanized honey bees in Mexico. J. Apic. Res. and Bee World 46, 295–300CrossRefGoogle Scholar
  34. Quezada-Euán J.J.G., Medina L.M. (1998) Hybridisation between European and Africanized honeybees (Apis mellifera L.) in tropical Yucatan, México. I. Morphometric changes in feral and managed colonies. Apidologie 29, 555–568CrossRefGoogle Scholar
  35. Rueppell, O., Bachelier, C., Fondrk, M.K., Page, R.E. (2007) Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp. Gerontol. 42, 1020–1032CrossRefPubMedPubMedCentralGoogle Scholar
  36. Santos, L.G.; Alves, M.L., Message, D., Pinto, F.A., Silva, M.V., Teixeira, E.W. (2014) Honey bee health in apiaries in the Vale do Paraíba, São Paulo State, Southeastern Brazil. Sociobiology 6 (13), 307–312Google Scholar
  37. Scheiner, R.; Abramson, C.I.; Brodschneider, R., Crailsheim, K., Farina, W. et al. (2013) Standard methods for mehavioural studies of Apis mellifera. J. Apicul. Res. 52 (4), 1–58CrossRefGoogle Scholar
  38. Seeley, T D. (1995) The Wisdom of the Hive. Harvard University Press, Cambridge, MA, USAGoogle Scholar
  39. SIAP-SAGARPA (2016) Abejas: población apícola 2006–2015, Colmenas [Online] (accessed on 19 October 17)
  40. Teixeira, E.W., dos Santos, L.G., Sattler, A., Message, D., Alves, F.M.T.L.M., Martins, F.M., Grassi-Sella, M.L., Francoy, T.M. (2013) Nosema ceranae has been present in Brazil for more than three decades infecting Africanized honey bees. J. Invert. Pathol. 114, 250–254CrossRefGoogle Scholar
  41. Therneau, T.M., Grambsch, P.M., Pankratz, V.S. (2003). Penalized survival models and frailty. J. Comput. Graph. Stat. 12, 156–175CrossRefGoogle Scholar
  42. Therneau, T.M., Lumley, T. (2015). Package “survival”. R. Top. Doc., 128 Google Scholar
  43. Vandame, R., Palacio, M.A. (2010) Preserved honey bee health in Latin America: a fragile equilibrium due to low-intensity agriculture and beekeeping? Apidologie 41, 243–255CrossRefGoogle Scholar
  44. Williams, G.R., Shutler, D., Little, C.M., Burgher-MacLellan, K.L., Rogers, R.E.L., (2011) The microsporidian Nosema ceranae, the antibiotic Fumagilin-B®, and western honey bee (Apis mellifera) colony strength. Apidologie 42 (1), 15–22CrossRefGoogle Scholar
  45. Wolf, S., McMahon D.P., Lim, K.S., Pull, C.D., Clark, S.J., Paxton, R.J., Osborne, J.L. (2014) So near and yeat so far: Harmonic radar reveals reduced homing ability of Nosema infected honeybees. PLoS One 9 (8), e103989CrossRefPubMedPubMedCentralGoogle Scholar
  46. Woyciechowski, M., Moron, D. (2009) Life expectancy and onset of foraging in the honeybee (Apis mellifera). Insectes Soc. 56, 193–201CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Departamento de ApiculturaCampus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán ApdoMeridaMexico

Personalised recommendations