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

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Abstract

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.

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References

  • 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 52:399–451

    Article  PubMed  Google Scholar 

  • 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 12:774–782

    Article  PubMed  Google Scholar 

  • Amdam GV, Omholt SW (2003) The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J Theor Biol 223:451–464

    Article  PubMed  CAS  Google Scholar 

  • 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 11:2284–2290

    Article  PubMed  CAS  Google Scholar 

  • Bailey L (1981) Honey bee pathology. Academic Press, London

    Google Scholar 

  • Campbell J, Kessler B, Mayack C, Naug D (2010) Behavioral fever in infected honeybees: parasitic manipulation or coincidental benefit? Parasitology 137:1487–1491

    Article  PubMed  Google Scholar 

  • 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 56:142–147

    Article  CAS  Google Scholar 

  • 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 101:204–209

    Article  Google Scholar 

  • 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 63:74–81

    Article  Google Scholar 

  • 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:1–11

  • Feder D, Mello CB, Garcia ES, Azambuja P (1997) Immune responses in Rhodnius prolixus: influence of nutrition and ecdysone. J Insect Physiol 43:513–519

    Article  PubMed  CAS  Google Scholar 

  • 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 57:217–222

    Article  Google Scholar 

  • 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 32:356–365

    Google Scholar 

  • Fries I (2009) Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 103:S73–S79

    Article  PubMed  Google Scholar 

  • Forsgren E, Fries I (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Vet Parasitol 170:212–217

    Article  PubMed  Google Scholar 

  • Gregory PG, Evans JD, Rinderer T, de Guzman L (2005) Conditional immune-gene suppression of honeybees parasitized by Varroa mites. J Insect Sci: 5:7

    Google Scholar 

  • 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 133:323–333

    Article  PubMed  Google Scholar 

  • Higes M, Martín R, Meana A (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92:93–95

    Article  PubMed  CAS  Google Scholar 

  • Higes M, García-Palencia P, Martín-Hernández R, Meana A (2007) Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J Invertebr Pathol 94:211–217

    Article  PubMed  Google Scholar 

  • 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 10:2659–2669

    Article  PubMed  Google Scholar 

  • 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 1:110–113

    Article  Google Scholar 

  • 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 1:495–498

    Article  Google Scholar 

  • Higes M, Martín-Hernández R, Meana A (2010) Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41:375–392

    Article  Google Scholar 

  • Huang WF, Jiang JH, Chen YW, Wang CH (2007) A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38:30–37

    Article  Google Scholar 

  • 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 7:293–300

    Article  Google Scholar 

  • 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 96:1–10

    Article  PubMed  Google Scholar 

  • Liu TP (1984) Ultrastructure of the midgut of the worker honey bee Apis mellifera heavily infected with Nosema apis. J Invertebr Pathol 44:282–291

    Article  Google Scholar 

  • Lloyd S (1995) Environmental influences on host immunity. In: Grenfell T, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, UK

    Google Scholar 

  • 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 26:495–502

    Article  Google Scholar 

  • 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 73:6331–6338

    Article  PubMed  Google Scholar 

  • May RM, Anderson RM (1990) Parasite–host coevolution. Parasitology 100:S89–S101

    Article  PubMed  Google Scholar 

  • Mayack C, Naug D (2009) Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J Invertebr Pathol 100:185–188

    Article  PubMed  Google Scholar 

  • Mayack C, Naug D (2010) Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. J Insect Physiol 56:1572–1575

    Article  PubMed  CAS  Google Scholar 

  • Milinski M (1984) Parasites determine a predator's optimal feeding strategy. Behav Ecol Sociobiol 15:35–37

    Article  Google Scholar 

  • Milinski M (1985) Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L) under competition for food. Behaviour 93:203–215

    Article  Google Scholar 

  • Moffet JO, Lawson FA (1975) Effect of Nosema-infection on O2 consumption by honey bees. J Econ Entomol 68:627–629

    Google Scholar 

  • Naug D (2009) Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol Conserv 142:2369–2372

    Article  Google Scholar 

  • Naug D, Gibbs A (2009) Behavioral changes mediated by hunger in honeybees infected with Nosema ceranae. Apidologie 40:595–599

    Article  Google Scholar 

  • Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol 5:673–677

    Article  CAS  Google Scholar 

  • Office International des Epizooties (OIE) (2008) Manual of standards for diagnostic test and vaccines [online]. http://www.oie.int/eng/normes/mmanual/2008. Accessed 20 June 2010

  • Paxton RJ (2010) Does infection by Nosema ceranae cause "Colony Collapse Disorder" in honey bees (Apis mellifera)? J Apic Res 49:80–84

    Article  Google Scholar 

  • 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 38:558–565

    Article  Google Scholar 

  • Pulkkinen K, Ebert D (2004) Host starvation decreases parasite load and mean host size in experimental populations. Ecology 85:823–833

    Article  Google Scholar 

  • Rinderer TE, Elliot K (1977) Influence of nosematosis on the hoarding behavior of the honeybee. J Invertebr Pathol 30:110–111

    Article  Google Scholar 

  • Rothe U, Nachtigall W (1989) Flight of the honey bee. J Comp Physiol B Biochem Syst Environ Physiol 158:739–749

    Article  Google Scholar 

  • Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50:529–551

    Article  PubMed  CAS  Google Scholar 

  • Siva-Jothy MT, Thompson JJW (2002) Short-term nutrient deprivation affects immune function. Physiol Entomol 27:206–212

    Article  Google Scholar 

  • Sokolova YY, Timoshenko SA, Issi VI (1988) Morphogenesis and ultrastructure of life cycle stages of Nosema mesnili (Microsporidia, Nosematidae). Citologiya 30:26–33

    Google Scholar 

  • Toth AL, Kantarovich S, Meisel AF, Robinson GE (2005) Nutritional status influences socially regulated foraging ontogeny in honey bees. J Exp Biol 208:4641–4649

    Article  PubMed  Google Scholar 

  • 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 102:7470–7475

    Article  PubMed  CAS  Google Scholar 

  • Wakelin D (1989) Nature and nurture: overcoming constraints on immunity. Parasitology 99:S21–S35

    Article  PubMed  Google Scholar 

  • Walkey M, Meakins RH (1970) An attempt to balance energy budget of a host-parasite system. J Fish Biol 2:361–372

    Article  Google Scholar 

  • 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 172–195

    Google Scholar 

  • Williams BAP (2009) Unique physiology of host-parasite interactions in microsporidia infections. Cell Microbiol 11:1551–1560

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Author contributions: MH, RM-H designed the research; MH, RM-H and CB carried out the assay and collected the data; LB and AM-S performed statistic studies; and MH, AM, C.M. and R.M-H. wrote the paper. RTA2009-00105-C02-01 national research project and MARM-FEAGA founds (Programa Nacional Apícola 2011-2013) provided research facilities and monetary support. We would like to thank to Almudena Cepero, Virginia Albendea, Carmen Abascal, Carmen Rogerio and Teresa Corrales for their technical support. We thank Dr. Naug for revision of the text.

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Authors and Affiliations

  1. Bee Pathology Laboratory, Centro Apícola Regional, JCCM, San Martín s/n, 19180, Marchamalo, Guadalajara, Spain

    Raquel Martín-Hernández, Cristina Botías & Mariano Higes

  2. Statistics Department, CTI, Consejo Superior Investigaciones Científicas, 28006, Madrid, Spain

    Laura Barrios

  3. Epidemiology Department, TRAGSEGA, Madrid, Spain

    Amparo Martínez-Salvador

  4. Animal Health Department, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040, Madrid, Spain

    Aránzazu Meana

  5. Department of Biology, Colorado State University, Fort Collins, CO, 80523, USA

    Christopher Mayack

Authors
  1. Raquel Martín-Hernández
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  2. Cristina Botías
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  3. Laura Barrios
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  4. Amparo Martínez-Salvador
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  5. Aránzazu Meana
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  6. Christopher Mayack
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  7. Mariano Higes
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Correspondence to Mariano Higes.

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Martín-Hernández, R., Botías, 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 109, 605–612 (2011). https://doi.org/10.1007/s00436-011-2292-9

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  • DOI: https://doi.org/10.1007/s00436-011-2292-9

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