Survival of honey bees (Apis mellifera) infected with Crithidia mellificae (Langridge and McGhee: ATCC® 30254™) in the presence of Nosema ceranae

  1. Higes, Mariano 1
  2. Rodríguez-García, Cristina 1
  3. Gómez-Moracho, Tamara 1
  4. Meana, Aranzazu 2
  5. Bartolomé, Carolina 3
  6. Maside, Xulio 3
  7. Barrios, Laura 4
  8. Martín-Hernández, Raquel 1
  1. 1 Junta de Comunidades de Castilla-La Mancha, España
  2. 2 Universidad Complutense de Madrid, España
  3. 3 Universidade de Santiago de Compostela, España
  4. 4 Consejo Superior Investigaciones Científicas, España
Mostrar afiliacións +
Revista:
Spanish journal of agricultural research

ISSN: 1695-971X,  2171-9292

Ano de publicación: 2016

Volume: 14

Número: 3

Tipo: Artigo

DOI: 10.5424/SJAR/2016143-8722 DIALNET GOOGLE SCHOLAR lock_openDialnet editor

Outras publicacións en: Spanish journal of agricultural research

Resumo

Crithidia mellificae, a trypanosomatid parasite of Apis mellifera, has been proposed to be one of the pathogens responsible for the serious honey bee colony losses produced worldwide in the last decade, either alone or in association with Nosema ceranae. Since this pathogenic effect contradicts the results of the experimental infections originally performed by Langridge and McGhee nearly 40 years ago, we investigated the potential linkage of this protozoan with colony decline under laboratory conditions. Nosema-free and trypanosomatid-free honey bees from three different colonies were experimentally infected with fresh C. mellificae spheroid forms (reference strain ATCC30254), with N. ceranae fresh spores and with both parasites at the same time. Replicate cages were kept at 27 °C and used to analyse survival. C. mellificae spheroid forms did not reduce significantly the survival of the worker bees (64.5% at 30 days post-infection vs. 77.8% for the uninfected bees used as controls; differences were non statistically significant) under these experimental conditions. In contrast, the cages infected with N. ceranae exhibited higher rates of mortality from the 20th day post-infection onwards, irrespective of the presence of C. mellificae, suggesting that the spheroid forms of the latter have no pathological effect on A. mellifera.

€ Ver financiamento

Información de financiamento

INIA-FEDER (RTA2013-00042-C10-06 and E-RTA2014-00003-C03).

Financiadores

    • RTA2013-00042-C10-06
    • E-RTA2014-00003-C03

Referencias bibliográficas

  • Cepero A, Gómez-Moracho T, Bernal JL, Del Nozal MJ, Bartolomé C, Maside X, Meana A, González-Porto AV, de Graaf DC, Martín-Hernández R, Higes M, 2014. Holistic screening of collapsing honey bee colonies in Spain: a case study. BMC Research Notes 7: 649. http://dx.doi.org/10.1186/1756-0500-7-649
  • Cornman RS, Tarpy DR, Chen Y, Jeffreys R, Lopez D, Pettis JS, vanEngelsdorp D, Evans JD, 2012. Pathogen webs in collapsing honey bee colonies. PLOS ONE 8: e43652. http://dx.doi.org/10.1371/journal.pone.0043562
  • Cox-Foster DL, Conlan S, Holmes E., Palacios E, Evans JD, et al., 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287. http://dx.doi.org/10.1126/science.1146498
  • Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P, 2012. Predictive markers of honey bee colony collapse. PLOS ONE 7(2): e32151. http://dx.doi.org/10.1371/journal.pone.0032151
  • Francis RM, Nielsen SL, Kryger P, 2013. Varroa-virus interaction in collapsing honey bee colonies. PLOS ONE 8(3):e57540. http://dx.doi.org/10.1371/journal.pone.0057540
  • Galanti N, Galindo M, Sabaj V, Espinoza I, Toro G, 1998. Histone genes in trypanosomatids. Parasitol Today 14: 64-70. http://dx.doi.org/10.1016/S0169-4758(97)01162-9
  • Higes M, Martín-Hernández R, Meana A, 2006. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92: 93-95. http://dx.doi.org/10.1016/j.jip.2006.02.005
  • Higes M, García-Palencia P, Botías C, Meana A, Martín-Hernández R, 2010. The differential development of microsporidia infecting worker honey bee (Apis mellifera) at increasing incubation temperature. Environ Microbiol Rep 2: 745-748. http://dx.doi.org/10.1111/j.1758-2229.2010.00170.x
  • Higes M, Juarranz Á, Dias-Almeida J, Lucena S, Botías C, Meana A, Garcia-Palencia P, Martín-Hernández R, 2013. Apoptosis in the pathogenesis of Nosema ceranae (Microsporidia: Nosematidae) in honey bees (Apis mellifera). Environ Microbiol Rep 5(4): 530-536. http://dx.doi.org/10.1111/1758-2229.12059
  • Huang WF, Solter L, Aronstein K, Huang Z, 2015. Infectivity and virulence of Nosema ceranae and Nosema apis in commercially available North American honey bees. Invertebr Pathol 124:107-113. http://dx.doi.org/10.1016/j.jip.2014.10.006
  • Knoll AJ, 1992. The early evolution of eukaryotes: a geological perspective. Science 256: 622-627. http://dx.doi.org/10.1126/science.1585174
  • Langridge D, McGhee R, 1967. Crithidia mellificae n. sp. An acidophilic trypanosomatid of de honey bee Apis mellifera. J Protozool 14(3): 485-487. http://dx.doi.org/10.1111/j.1550-7408.1967.tb02033.x
  • Martín-Hernández R, Meana A, García-Palencia, Marín, Botías C, Garrido-Bailó E, Barrios L, Higes M, 2009. Effect of temperature on the biotic potential of honeybee microsporidia. Appl Environ Microbiol 75 (8): 2554-2557. http://dx.doi.org/10.1128/AEM.02908-08
  • Martín-Hernández R, Botías C, Barrios L, Martínez-Salvador A, Meana A, Mayack C, Higes M, 2011. Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honey bees (Apis mellifera). Parasitol Res 109: 605-612. http://dx.doi.org/10.1007/s00436-011-2292-9
  • Martín-Hernández R, Botías C, Garrido Bailón E, Martínez-Salvador A, Prieto L, Meana A, Higes M, 2012. Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environ Microbiol 14 (8): 2127-2138. http://dx.doi.org/10.1111/j.1462-2920.2011.02645.x
  • Meeus I, De Graaf DC, Jans K, Smagghe G, 2010. Multiplex PCR detection of slowly-evolving trypanosomatids and neogregarines in bumblebees using broad-range primers. J Appl Microbiol 109: 107-115.
  • Milbrath MO, van Tran T, W-F Huang L F, Solter DR, Tarpy F, Z Huang, 2015. Comparative virulence and competition between Nosema apis and Nosema ceranae in honey bees (Apis mellifera). J Invertebr Pathol 125: 9-15. http://dx.doi.org/10.1016/j.jip.2014.12.006
  • Popp M, Lattorff HMG, 2011. A quantitative in vitro cultivation technique to determine cell number and growth rates in strains of Crithidia bombi (Trypanosomatidae), a parasite of bumblebees. J Eukaryotic Microbiol 58: 7-10. http://dx.doi.org/10.1111/j.1550-7408.2010.00514.x
  • Ravoet J, Maharramov J. Meeus I, De Smet L, Wenseleers T, Smagghe G, de Graaf DC, 2013. Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PLOS ONE 8: e72443. http://dx.doi.org/10.1371/journal.pone.0072443
  • Ravoet J, Schwarz RS, Descamps T, Yañez O, Torkaz OC, Martín-Hermández R, Bartolomé C, De Smert L, Higes M, Wenseleers T, Schmid-Hempel R, Neuman P, Kadowaki T, Evans JD, de Graaf D, 2015. Differential diagnosis of the honey bee trypanosomatids Crithidia mellificae and Lotmaria passim. J Invertebr Pathol 130: 21-27. http://dx.doi.org/10.1016/j.jip.2015.06.007
  • Runckel C, Flenniken M, Engel JC, Ruby JG, Ganem D, Andino R, DeRisi JL, 2011. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS ONE 6: e20656. http://dx.doi.org/10.1371/journal.pone.0020656
  • Runckel C, DeRisi J, Flenniken ML, 2014. A draft genome of the honey bee trypanosomatid parasite Crithidia mellificae. PLOS ONE 9: e95057. http://dx.doi.org/10.1371/journal.pone.0095057
  • Schmid-Hempel R, Tognazzo M, 2010. Molecular divergence defines two distinct lineages of Crithidia bombi (Trypanosomatidae), parasites of bumblebees. J Eukaryotic Microbiol 57 (4): 337-345. http://dx.doi.org/10.1111/j.1550-7408.2010.00480.x
  • Schwarz RS, Evans JD, 2013. Single and mixed-species trypanosome and microsporidia infections elicit distinct, ephemeral cellular and humoral immune responses in honey bees. Dev Comp Immunol 2013 40 (3-4): 300-310. http://dx.doi.org/10.1016/j.dci.2013.03.010
  • Schwarz RS, Bauchan G., Murphy CA, Ravoet J, De Graaf DC. Evans JD, 2015. Characterization of two species of trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, 1967 and Lotmaria passim n. gen., n. sp. J Eukaryotic Microbiol 10: 1-17.
  • Vanengelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, Frazier M, Frazier J, Cox-Foxter D, Chen Y et al., 2009. Colony collapse disorder: a descriptive study. PLoS ONE 4: e6481. http://dx.doi.org/10.1371/journal.pone.0006481
  • Williams GR, Shutler D, Burgher-MacLellan K., Rogers RE, 2014. Infra-population and community dynamics of the parasites Nosema apis and Nosema ceranae, and consequences for honey bee (Apis mellifera) hosts. PLOS ONE 9: e99465. http://dx.doi.org/10.1371/journal.pone.0099465
Fonte de datos: Dialnet