275
Views
3
CrossRef citations to date
0
Altmetric
NOSEMA AND RELATIVES

Presence of Lotmaria passim, Crithidia mellificae and Nosema spp. in differently aged Apis mellifera brood

ORCID Icon, &
Pages 287-296 | Received 14 Dec 2021, Accepted 21 Feb 2022, Published online: 21 Apr 2022

References

  • Anderson, K. E., Sheehan, T. H., Eckholm, B. J., Mott, B. M., & DeGrandi-Hoffman, G. (2011). An emerging paradigm of colony health: Microbial balance of the honey bee and hive (Apis mellifera). Insectes Sociaux, 58(4), 431–444. https://doi.org/10.1007/s00040-011-0194-6
  • Arismendi, N., Bruna, A., Zapata, N., & Vargas, M. (2016). PCR-specific detection of recently described Lotmaria passim (Trypanosomatidae) in Chilean apiaries. Journal of Invertebrate Pathology, 134, 1–5. https://doi.org/10.1016/j.jip.2015.12.008
  • Arismendi, N., Caro, S., Castro, M. P., Vargas, M., Riveros, G., & Venegas, T. (2020). Impact of mixed infections of gut parasites Lotmaria passim and Nosema ceranae on the Lifespan and immune-related biomarkers in Apis mellifera. Insects, 11(7), 420. https://doi.org/10.3390/insects11070420
  • Arismendi, N., Riveros, G., Zapata, N., Smagghe, G., González, C., & Vargas, M. (2021). Occurrence of bee viruses and pathogens associated with emerging infectious diseases in native and non-native bumble bees in southern Chile. Biological Invasions, 23(4), 1175–1115. https://doi.org/10.1007/s10530-020-02428-w
  • Barrett, J., Vardulaki, K., Conlon, C., Cooke, J., Daza-Ramirez, P., Evans, E., Hawkey, P., Herbrecht, R., Marks, D., Moraleda, J., Park, G., Senn, S., & Viscoli, C. (2003). Systematic review of the antifungal effectiveness and tolerability of amphotericin B formulations. Clinical Therapeutics, 25(5), 1295–1320. https://doi.org/10.1016/S0149-2918(03)80125-X
  • Calderone, N. W. (2012). Insect pollinated crops, insect pollinators and US agriculture: Trend analysis of aggregate data for the period 1992–2009. PLoSOne, 7, 24–28. https://doi.org/10.1371/journal.pone.0037235.
  • Castelli, L., Branchiccela, B., Invernizzi, C., Tomasco, I., Basualdo, M., Rodriguez, M., Zunino, P., & Antúnez, K. (2019). Detection of Lotmaria passim in Africanized and European honey bees from Uruguay, Argentina and Chile. Journal of Invertebrate Pathology, 160, 95–97. https://doi.org/10.1016/j.jip.2018.11.004
  • Chauzat, M. P., Cauquil, L., Roy, L., Franco, S., Hendrikx, P., & Ribière-Chabert, M. (2013). Demographics of the European apicultural industry. PLoSONE 8, 8(11), e79018. https://doi.org/10.1371/journal.pone.0079018e79018
  • Cilia, G., Cardaio, I., dos Santos, P. E. J., Ellis, J. D., & Nanetti, A. (2018). The first detection of Nosema ceranae (Microsporidia) in the small hive beetle, Aethina tumida Murray (Coleoptera: Nitidulidae). Apidologie, 49(5), 619–624. https://doi.org/10.1007/s13592-018-0589-8
  • Cilia, G., Fratini, F., Tafi, E., Mancini, S., Turchi, B., Sagona, S., Cerri, D., Felicioli, A., & Nanetti, A. (2021). Changes of Western honey bee Apis mellifera ligustica (Spinola, 1806) ventriculus microbial profile related to their in-hive tasks. Journal of Apicultural Research, 60(1), 198–202. https://doi.org/10.1080/00218839.2020.1830259
  • Cornman, R., S., Tarpy, D., R., Chen, Y., Jeffreys, L., Lopez, D., Jeffery, S., Pettis, J. S., vanEngelsdorp, D., & Evans, J., D. (2012). Pathogen webs in collapsing Honey Bee Colonies. PLoS ONE, 7(8): e43562. https://doi.org/10.1371/journal.pone.0043562
  • Czekońska, K. (2000). The influence of Nosema apis on young honey bee queens and transmission of the disease from queens to workers. Apidologie, 31, 701–706.
  • D’Alvise, P., Seeburger, V., Gihring, K., Kieboom, M., & Hasselmann, M. (2019). Seasonal dynamics and co-occurrence patterns of honey bee pathogens revealed by high-throughput RT-qPCR analysis . Ecology and Evolution, 9(18), 10241–10252. https://doi.org/10.1002/ece3.5544
  • de Landa, G. F., Porrini, M. P., Revainera, P., Porrini, D. P., Farina, J., Correa-Benítez, A., Maggi, M. D., Eguaras, M. J., & Quintana, S. (2021). Pathogens detection in the small hive beetle (Aethina tumida (Coleoptera: Nitidulidae)). Neotropical Entomology, 50(2), 312–315. https://doi.org/10.1007/s13744-020-00812-8
  • Fenoy, S., Rueda, C., Higes, M., Martin-Hernandez, R., & Aguila, C. (2009). High-level resistance of Nosema ceranae, a parasite of the honey bee, to temperature and desiccation. Applied and Environmental Microbiology, 75(21), 6886–6889. https://doi.org/10.1128/AEM.01025-09
  • Gegear, R. J., & Laverty, T. M. (2005). Flower constancy in bumble bees: A test of the trait variability hypothesis. Animal Behaviour, 69(4), 939–949. https://doi.org/10.1016/j.anbehav.2004.06.029
  • Genersch, E. (2010). Honey bee pathology: Current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology, 87(1), 87–97. https://doi.org/10.1007/s00253-010-2573-8
  • Gliński, Z., & Rzedzicki, J. (1993). Choroby pszczół, PWN Warszawa
  • Gómez-Moracho, T., Buendía-Abad, M., Benito, M., García-Palencia, P., Barrios, L., Bartolomé, C., Maside, X., Meana, A., Jiménez-Antón, M. D., Olías-Molero, A. I., Alunda José, M., Martín-Hernández, R., & Higes, M. (2020). Experimental evidence of harmful effects of Crithidia mellificae and Lotmaria passim on honey bees. International Journal for Parasitology, 50(13), 1117–1125. https://doi.org/10.1016/j.ijpara.2020.06.009
  • Higes, M., Garcia-Palencia, P., Martin-Hernández, R., & Meana, A. (2007). Experimental infection of Apis mellifera honey bees with Nosema ceranae (Microsporidia). Journal of Invertebrate Pathology, 94(3), 211–217. https://doi.org/10.1016/j.jip.2006.11.001
  • Higes, M., Juarranz, Á., Dias-Almeida, J., Lucena, S., Botías, C., Meana, A., García-Palencia, P., & Martín-Hernández, R. (2013). Apoptosis in the pathogenesis of Nosema ceranae (Microsporidia: Nosematidae) in honey bees (Apis mellifera)). Environmental Microbiology Reports, 5(4), 530–536. https://doi.org/10.1111/1758-2229.12059
  • Hroncova, Z., Havlik, J., Killer, J., Doskocil, I., Tyl, J., Kamler, M., Titera, D., Hakl, J., Mrazek, J., Bunesova, V., & Rada, V. (2015). Variation in honey bee gut microbial diversity affected by ontogenetic stage: Age and geographic location. PLoS ONE 10(3): e0118707. https://doi.org/10.1371/journal.pone.0118707
  • Kwong, W. K., Mancenido, A. L., & Moran, N. A. (2017). Immune system stimulation by the native gut microbiota of honey bees. Royal Society Open Science, 4(2), 170003. PMID: 28386455; PMCID: PMC536727 https://doi.org/10.1098/rsos.170003
  • Langridge, D. F., & McGhee, R. B. (1967). Crithidia mellificae n. sp. an acidophilic trypanosomatid of the honey bee Apis mellifera. The Journal of Protozoology, 14(3), 485–487. https://doi.org/10.1111/j.1550-7408.1967.tb02033
  • Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailón, E., & Higes, M. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae. Applied and Environmental Microbiology, 73(20), 6331–6338. https://doi.org/10.1128/AEM.00270-07
  • Maslov, D., Votýpka, J., Yurchenko, V., & Lukeš, J. (2013). Diversity and phylogeny of insect trypanosomatids: All that is hidden shall be revealed. Trends in Parasitology, 29(1), 43–52. https://doi.org/10.1016/j.pt.2012.11.001
  • Michalczyk, M., Bancerz-Kisiel, A., & Sokół, R. (2020). Lotmaria passim as third parasite gastrointestinal tract of honey bees living in tree trunk. Journal of Apicultural Science, 64(1), 143–151. https://doi.org/10.2478/jas-2020-0012
  • Michalczyk, M., & Sokół, R. (2018). Estimation of the influence of selected products on co-infection with N. apis/N. ceranae in Apis mellifera using real-time PCR. Invertebrate Reproduction & Development, 62(2), 92–97. https://doi.org/10.1080/07924259.2018.1433726
  • Morse, R. A., & Nowogrodzki, R. (1990). Honey bee pests, predators and diseases. Cornell University Press.
  • Nanetti, A., Ellis, J. D., Cardaio, I., & Cilia, G. (2021). Detection of Lotmaria passim, crithidia mellificae and replicative forms of deformed wing virus and Kashmir bee virus in the small hive beetle (Aethina tumida). Pathogens, 10(3), 372. https://doi.org/10.3390/pathogens10030372
  • Plischuk, S., Fernández de Landa, G., Revainera, P., Quintana, S., Pocco, M. E., Cigliano, M. M., & Lange, C. E. (2020). Parasites and pathogens associated with native bumble bees (Hymenoptera: Apidae: Bombus spp.) from highlands in Bolivia and Peru. Stud. Neotropical Fauna and Environment, 56(2), 93–98. https://doi.org/10.1080/01650521.2020.1743551
  • Plischuk, S., & Lange, C. E. (2016). Bombus brasiliensis Lepeletier (Hymenoptera, Apidae) infected with Nosema ceranae (Microsporidia). Revista Brasileira de Entomologia, 60(4), 347–351. https://doi.org/10.1016/j.rbe.2016.06.003
  • Plischuk, S., Martín-Hernández, R., Prieto, L., Lucía, M., Botías, C., Meana, A., Abrahamovich, A. H., Lange, C., & Higes, M. (2009). South American native bumble bees (Hymenoptera: Apidae) infected by Nosema ceranae (Microsporidia), an emerging pathogen of honey bees (Apis mellifera). Environmental Microbiology Reports, 1(2), 131–135. https://doi.org/10.1111/j.1758-2229.2009.00018.x
  • Porrini, C., Mutinelli, F., Bortolotti, L., Granato, A., Laurenson, L., Roberts, K., Gallina, A., Silvester, N., Medrzycki, P., Renzi, T., Sgolastra, F., & Lodesani, M. (2016). The status of honey bee health in Italy: Results from the nationwide bee monitoring network. PLoS One, 11(5), e0155411. https://doi.org/10.1371/journal.pone.0155411
  • Quintana, S., Plischuk, S., Brasesco, C., Revainera, P., Genchi García, M. L., Bravi, M. E., Reynaldi, F., Eguaras, M., & Maggi, M. (2021). Lotmaria passim (Kinetoplastea: Trypanosomatidae) in honey bees from Argentina. Parasitology International, 81, 102244–105769. https://doi.org/10.1016/j.parint.2020.102244
  • Ravoet, J., Maharramov, J., Meeus, I., de Smet, L., Wenseleers, T., Smagghe, G., & de Graaf, D. C. (2013). Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PloS One, 8(8), e72443. https://doi.org/10.1371/journal.pone.0072443
  • Retschnig, G., Williams, G. R., Schneeberger, A., & Neumann, P. (2017). Cold ambient temperature promotes Nosema spp. intensity in honey bees (Apis mellifera). Insects, 8(1), 20. https://doi.org/10.3390/insects8010020
  • Rodríguez, M., Vargas, M., Antúnez, K., Gerding, M., Castro, F. O., Zapata, N., & Chilean, J. (2014). Prevalence and phylogenetic analysis of honey bee viruses in the Biobío Region of Chile and their association with other honey bee pathogens. Chilean Journal of Agricultural Research, 74(2), 170–177. https://doi.org/10.4067/S0718-58392014000200007
  • Runckel, C., Flenniken, M. L., Engel, J. C., Ruby, J. G., Ganem, D., Andino, R., & DeRisi, J. L. (2011). Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One, 6(6), e20656. https://doi.org/10.1371/journal.pone.0020656
  • Schwarz, R. S., Bauchan, G. R., Murphy, C., Ravoet, J., de Graaf, D. C., & Evans, J. D. (2015). Characterization of two species of Trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, and Lotmaria passim n. gen., n. sp. The Journal of Eukaryotic Microbiology, 62(5), 567–583. https://doi.org/10.1111/jeu.12209
  • Schwarz, R. S., & Evans, J. D. (2013). Single and mixed-species trypanosome and microsporidia infections elicit distinct, ephemeral cellular and humoral immune responses in honey bees. Developmental and Comparative Immunology, 40(3-4), 300–310. https://doi.org/10.1016/j.dci.2013.03.01
  • Simon-Delso, N., Amaral-Rogers, V., Belzunces, L. P., Bonmatin, J. M., Chagnon, M., Downs, C., Furlan, L., Gibbons, D. W., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D. P., Krupke, C. H., Liess, M., Long, E., McField, M., Mineau, P., Mitchell, E. A. D., Morrissey, C. A., … Wiemers, M. (2015). Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environmental Science and Pollution Research International, 22(1), 5–34. https://doi.org/10.1007/s11356-014-3470-y
  • Sokół, R., & Michalczyk, M. (2012). Detection of Nosema spp. in worker bees of different ages during the flow season. Journal of Apicultural Science, 56(2), 19–25. https://doi.org/10.2478/v10289-012-0020-z
  • Sokół, R., Michalczyk, M., & Michołap, P. (2018). Preliminary studies on the occurrence of honey bee pathogens in the national bumble population. Annal of Parasitology, 64, 385–390.
  • Stevanovic, J., Schwarz, R. S., Vejnovic, B., Evans, J. D., Irwin, R. E., Glavinic, U., & Stanimirovic, Z. (2016). Species-specific diagnostics of Apis mellifera trypanosomatids: A nine-year survey (2007–2015) for trypanosomatids and microsporidians in Serbian honey bees. Journal of Invertebrate Pathology, 139, 6–11. https://doi.org/10.1016/j.jip.2016.07.001
  • Szalanski, A. L., Trammel, C. E., Tripodi, A. D., Cleary, D., Rusert, L., & Downey, D. (2016). Molecular diagnostics of the honey bee parasites Lotmaria passim and Crithidia spp.(Trypanosomatidae) using multiplex PCR. Florida Entomologist, 99(4), 793–795. https://doi.org/10.1653/024.099.0438
  • Tritschler, M., Retschnig, G., Yañez, O., Williams, G. R., & Neumann, P. (2017). Host sharing by the honey bee parasites Lotmaria passim and Nosema ceranae. Ecology and Evolution, 7(6), 1850–1857. https://doi.org/10.1002/ece3.2796
  • Vejnovic, B., Stevanovic, J., Schwarz, R. S., Aleksic, N., Mirilovic, M., Jovanovic, N. M., & Stanimirovic, Z. (2018). Quantitative PCR assessment of Lotmaria passim in Apis mellifera colonies co-infected naturally with Nosema ceranae. Journal of Invertebrate Pathology, 151, 76–81. https://doi.org/10.1016/j.jip.2017.11.003
  • Webster, T., Pomper, K., Hunt, G., Thacker, E., & Jones, S. (2004). Nosema apis infection in worker and queen Apis mellifera. Apidologie, 35(1), 49–54. https://doi.org/10.1051/apido:2003063
  • Xu, G., Palmer-Young, E., Skyrm, K., Daly, T., Sylvia, M., Averill, A., & Rich, S. (2018). Triplex real-time PCR for detection of Crithidia mellificae and Lotmaria passim in honey bees. Parasitology Research, 117(2), 623–628. https://doi.org/10.1007/s00436-017-5733-2

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.