735
Views
32
CrossRef citations to date
0
Altmetric
Pathology and parasitology

Promising antimicrobial activity against the honey bee parasite Nosema ceranae by methanolic extracts from Chilean native plants and propolis

, , ORCID Icon, &
Pages 522-535 | Received 22 Oct 2017, Accepted 09 Mar 2018, Published online: 06 Apr 2018

References

  • Antúnez, K., Harriet, J., Gende, L., Maggi, M., Eguaras, M., & Zunino, P. (2008). Efficacy of natural propolis extract in the control of American Foulbrood. Veterinary Microbiology, 131, 324–331.10.1016/j.vetmic.2008.04.011
  • Araneda, X., Cumian, M., & Morales, D. (2015). Distribution, epidemiological characteristics and control methods of the pathogen Nosema ceranae Fries in honey bees Apis mellifera L. (Hymenoptera, Apidae). Archivos de Medicina Veterinaria, 47, 129–138.10.4067/S0301-732X2015000200002
  • Barrientos, L., Herrera, C.L., & Montenegro, G. (2013). Chemical and botanical characterization of Chilean propolis and biological activity on cariogenic bacteria Streptococcus mutans and Streptococcus sobrinus. Brazilian Journal of Microbiology, 44, 577–585.10.1590/S1517-83822013000200038
  • Bastos, E.M.A.F., Simone, M., Macedo, D., Soares, A.E., & Spivak, M. (2008). In vitro study of the antimicrobial activity of Brazilian propolis against Paenibacillus larvae. Journal of Invertebrate Pathology, 97, 273–281.10.1016/j.jip.2007.10.007
  • Botías, C., Martín-Hernández, R., Barrios, A., Meana, A., & Higes, M. (2013). Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Veterinary Research, 44, 25.10.1186/1297-9716-44-25
  • Borba, R.S., Klyczek, K.K., Mogen, K.L., & Spivak, M. (2015). Seasonal benefits of a natural propolis envelope to honey bee immunity and colony health. Journal of Experimental Biology, 218, 3689–3699.10.1242/jeb.127324
  • Bravo, J., Carbonell, V., Sepúlveda, B., Delporte, C., Valdovinos, C.E., Martín-Hernández, R., & Higes, M. (2017). Antifungal activity of the essential oil obtained from Cryptocarya alba against infection in honey bees by Nosema ceranae. Journal of Invertebrate Pathology, 149, 141–147.10.1016/j.jip.2017.08.012
  • Chen, Y., Evans, J.D., Murphy, C., Gutell, R., Zuker, M., Gundensen-Rindal, D., & Pettis, J.S. (2009). Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. Journal of Eukaryotic Microbiology, 56, 142–147.10.1111/jeu.2009.56.issue-2
  • 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. Journal of Invertebrate Pathology, 97, 186–188.10.1016/j.jip.2007.07.010
  • Cushnie, T.P.T., & Lamb, A.J. (2005). Antimicrobial activity of flavonoids. International Journal of Antimicrobial Agents, 26, 343–356.10.1016/j.ijantimicag.2005.09.002
  • Damiani, N., Fernández, N.J., Porrini, M.P., Gende, L.B., Álvarez, E., Buffa, F., … Eguaras, M.J. (2014). Laurel leaf extracts for honey bee pest and disease management: Antimicrobial, microsporicidal, and acaricidal activity. Parasitology Research, 113, 701–709.10.1007/s00436-013-3698-3
  • Damiani, N., Porrini, M.P., Lancia, J.P., Álvarez, E., Garrido, P.M., … Eguaras, M.J. (2017). Effect of propolis oral intake on physiological condition. Journal of Apicultural Science, 61, 193–202.
  • Fleming, J.C., Schmehl, D.R., & Ellis, J.D. (2015). Characterizing the impact of commercial pollen substitute diets on the level of Nosema spp. in honey bees (Apis mellifera L.). PLoS One, 10(7), e0132014. doi:10.1371/journal.pone.0132014
  • Fries, I., Chauzat, M.-P., Chen, Y.-P., Doublet, V., Genersch, E., Gisder, S., … Williams, G.R. (2013). Standard methods for Nosema research. In V. Dietemann, J. D. Ellis, & P. Neumann (Eds), The COLOSS BEEBOOK: Volume II: Standard methods for Apis mellifera pest and pathogen research. Journal of Apicultural Research, 52(1). doi:10.3896/IBRA.1.52.1.14
  • Gisder, S., & Genersch, E. (2013). Molecular differentiatition of Nosema apis and Nosema ceranae base on species-specific sequence differences in a protein coding gene. Journal of Invertebrate Pathology, 113, 1–6.10.1016/j.jip.2013.01.004
  • Gisder, S., Hedtke, K., Möckel, N., Frielitz, M.-C., Linde, A., & Genersch, E. (2010). Five-year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae? Applied and Environmental Microbiology, 76, 3032–3038.10.1128/AEM.03097-09
  • Graystock, P., Goulson, D., & Hughes, W.O.H. (2015). Parasites in bloom: Flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proceedings of the Royal Society, B, 282, 20151371.10.1098/rspb.2015.1371
  • Hegazi, A.G., Abd El Hady, F.K., & Abd Allah, F.A. (2000). Chemical composition and antimicrobial activity of European propolis. Zeitschrift für Naturforschung C, 55, 70–75.
  • Higes, M., Martín, R., & Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honey bees in Europe. Journal of Invertebrate Pathology, 92, 93–95.10.1016/j.jip.2006.02.005
  • Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A.V., García-Palencia, P., Meana, A., … Bernal, J.L. (2009). Honey bee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Report, 1, 110–113.10.1111/emi4.2009.1.issue-2
  • Higes, M., Martín-Hernández, R., & Meana, A. (2010). Nosema ceranae in Europe: An emergent type C nosemosis. Apidologie, 41, 375–392.10.1051/apido/2010019
  • Higes, M., Meana, A., Bartolomé, C., Botías, C., & Martín-Hernández, R. (2013). Nosema ceranae (Microsporida), a controversial 21st century honey bee pathogen. Environmental Microbiology Report, 5, 17–29.10.1111/emi4.2013.5.issue-1
  • Hinojosa, A., & González, D. (2004). Prevalencia de para´sitos en Apis mellifera en colmenares del secano costero e interior de la VI Regio´ n, hile [Prevalence of parasites i Apis mellifera L. in beehives of dry coastal and interior of sixth region, Chile]. Parasitologı´a Latinoamericana, 59, 137–141.
  • Holm, S. (1979). A simple sequential rejective method procedure. Scandinavian Journal of Statistics, 6, 65–70.
  • Huang, S., Zhang, C.-P., Wang, K., Li, G.Q., & Hu, F.L. (2014). Recent advances in the chemical composition of propolis. Molecules, 19, 19610–19632.10.3390/molecules191219610
  • Huang, W.-F., Jiang, J.-H., Chen, Y.-W., & Wang, C.-H. (2007). A Nosema ceranae isolate from the honey bee Apis mellifera. Apidologie, 38, 30–37.10.1051/apido:2006054
  • Huang, W.-F., & Solter, L.F. (2013). Comparative development and tissue tropism of Nosema apis and Nosema ceranae. Journal of Invertebrate Pathology, 113, 35–51.10.1016/j.jip.2013.01.001
  • Huang, W.-F., Solter, L.F., Yau, P.M., & Imai, B.S. (2013). Nosema ceranae escapes fumagillin control in honey bees. PLoS Pathology, 9, e1003185. doi.10.1371/journal.ppat.1003185
  • Huang, W.-F., Solter, L., Aronstein, K., & Huang, Z. (2015). Infectivity and virulence of Nosema ceranae and Nosema apis in commercially available North American honey bees. Journal of Invertebrate Pathology, 124, 107–113.10.1016/j.jip.2014.10.006
  • Invernizzi, C., Abud, C., Tomasco, I.H., Harriet, J., Ramallo, G., Campá, J., … Mendoza, Y. (2009). Presence of Nosema ceranae in honey bees (Apis mellifera) in Uruguay. Journal of Invertebrate Pathology, 101, 150–153.10.1016/j.jip.2009.03.006
  • Jack, C.J., Uppala, S.S., Lucas, H.L., & Sagili, R.R. (2016). Effects of pollen dilution on infection of Nosema ceranae in honey bees. Journal of Insect Physiology, 87, 12–19.10.1016/j.jinsphys.2016.01.004
  • Kim, J.H., Park, J.K., & Lee, J.K. (2016). Evaluation of antimicrosporidian activity of plant extracts on Nosema ceranae. Journal of Apicultural Science, 60, 167–178. doi:10.1515/jas-2016-0027
  • Klee, J., Besana, A.M., Genersch, E., Gisder, S., Nanetti, A., Tam, D.Q., … Paxton, R.J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. Journal of Invertebrate Pathology, 96, 1–10.10.1016/j.jip.2007.02.014
  • Johnson, B.R. (2010). Division of labor in honey bees: Form, function, and proximate mechanisms. Behavioral Ecology and Sociobiology, 64, 305–316.10.1007/s00265-009-0874-7
  • Maistrello, L., Lodesani, M., Costa, C., Leonardi, F., Marati, G., Caldon, M., … Granato, A. (2008). Screening of natural compounds for the control of nosema disease in honey bees (Apis mellifera). Apidologie, 39, 436–444.10.1051/apido:2008022
  • Martín-Hernández, R., Botías, C., Bailón, E.G., Martínez-Salvador, A., Prieto, L., … Higes, M. (2012). Microsporidia infecting Apis mellifera: Coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environmental Microbiology, 14, 2127–2138.10.1111/j.1462-2920.2011.02645.x
  • Paxton, R.J., 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, 558–565.10.1051/apido:2007037
  • Peña-Cerda, M., Arancibia-Radich, J., Valenzuela-Bustamante, P., Pérez-Arancibia, R., Barriga, A., Seguel, I., … Delporte, C. (2017). Phenolic composition and antioxidant capacity of Ugni molinae Turcz. leaves of different genotypes. Food Chemestry, 215, 219–227.10.1016/j.foodchem.2016.07.159
  • Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, 2003–2007.
  • Porrini, M.P., Garrido, P.M., & Eguaras, M.J. (2013). Individual feeding of honey bees: Modification of the Rinderer technique. Journal of Apicultural Research, 52(5), 194–195. doi: 10.3896/IBRA.1.52.5.04
  • Porrini, M.P., Garrido, P.M., Gende, L.B., Rossini, C., Hermidac, L., Marcángelia, J.A., & Eguaras, M.J. (2017). Oral administration of essential oils and main components: Study on honey bee survival and Nosema ceranae development. Journal of Apicultural Research, 56(5), 616–624. doi: 10.1080/00218839.2017.1348714
  • Porrini, M.P., Fernández, N.J., Garrido, P.M., Gende, L.B., Medici, S.K., & Eguares, M.J. (2011). In vivo evaluation of antiparasitic activity of plant extracts on Nosema ceranae (Microsporidia). Apidologie, 42, 700–707.10.1007/s13592-011-0076-y
  • Porrini, M.P., Sarlo, E.G., Medici, S.K., Garrido, P.M., Porrini, D.P., … Eguares, M.J. (2011). Nosema ceranae development in Apis mellifera: Influence of diet and infective inoculums. Journal of Apicultural Research, 50, 35–41.10.3896/IBRA.1.50.1.04
  • Romanucci, V., D’Alonzo, D., Guaragna, A., Di Marino, C., Davinelli, S., Scapagnini, G., … Zarrelli, A. (2016). Bioactive compounds of Aristotelia chilensis Stuntz and their pharmacological effects. Current Pharmaceutical Biotechnology, 17, 513–523.10.2174/1389201017666160114095246
  • Rubilar, M., Gutiérrez, C., Villarroel, M., & Shene, C. (2010). Influence of separation conditions on antimicrobial activity of polyphenolic fractions from murta leaves extract. CyTA – Journal of Food, 8, 139–149.10.1080/19476330903274161
  • Saavedra, N., Barrientos, L., Herrera, C., Alvear, M., Montenegro, G., & Salazar, L.A. (2011). Effect of Chilean propolis on cariogenic Lactobacillus fermentum bacteria. Ciencia e Investigación Agraria, 38, 117–125.
  • SAG. (2010). Informe de caso de Nosema ceranae en la regio´n del Bı´o Bı´o, octubre de 2009 [Case report of Nosema ceranae in the BioBío region, October 2009]. Retrieved from http://www.sag.cl/sites/default/files/informe_caso_nosema_ceranae_biobio_2009.pdf
  • Shene, C., Canquil, N., Jorquera, M., Pinelo, M., Rubilar, M., Acevedo, F., … Mardones, C. (2012). In vitro activity on human gut bacteria of murta leaf extracts (Ugni molinae Turcz.), a native plant from Southern Chile. Journal of Food Science, 77, M323–M329.10.1111/j.1750-3841.2012.02692.x
  • Shene, C., Reyes, A., Villarroel, M., Sineiro, J., Pinelo, M., & Rubilar, M. (2009). Plant location and extraction procedure strongly alter the antimicrobial activity of murta extracts. European Food Research and Technology, 228, 467–475.10.1007/s00217-008-0954-3
  • Simone-Finstrom, M., & Spivak, M. (2010). Propolis and bee health: The natural history and significance of resin use by honey bees. Apidologie, 41, 295–311.10.1051/apido/2010016
  • Singleton, V.L., & Rossi, J.A. (1965). Colorimentry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enolology And Viticulture, 16, 144–158.
  • Suwannapong, G., Maksong, S., & Benbow, M.E. (2011). Stingless bee propolis effects on experimental infection of Apis florea with Nosema ceranae. Journal of Agricultural Science and Technology A, 1, 818–825.
  • Tlak, I., Kozaric, Z., Berta, D., Nejedli, S., & Petrinec, Z. (2011). Effect of the herbal preparation Nozevit on the mid-gut structure of honey bees (Apis mellifera) infected with Nosema sp. spores. Veterinarni Medicina, 56, 344–351.
  • Teixeira, E.W., dos Santos, L.G., Sattler, A., Message, D., Alves, M., Martins, M.F., … Francoy, M. (2013). Nosema ceranae has been present in Brazil for more than three decades infecting Africanized honey bees. Journal of Invertebrate Pathology, 114, 250–254.10.1016/j.jip.2013.09.002
  • van den Heever, J.P., Thompson, T.S., Curtis, J.M., Ibrahim, A., & Pernal, S. (2014). Fumagillin: An overview of recent scientific advances and their significance for apiculture. Journal of Agricultural Food Chemestry, 62, 2728–2737.10.1021/jf4055374
  • van den Heever, J.P., Thompson, T.S., Curtis, J.M., & Pernal, S. (2015). Stability of dicyclohexylamine and fumagillin in honey. Food Chemestry, 179, 152–158.10.1016/j.foodchem.2015.01.111
  • Vargas, M., Arismendi, N., Riveros, G., Zapata, N., Bruna, A., Vidal, M., … Gerding, M. (2017). Viral and intestinal diseases detected in Apis mellifera in Central and Southern Chile. Chilean Journal of Agricultural Research, 77, 243–249.10.4067/S0718-58392017000300243
  • Veloz, J.J., Saavedra, N., Lillo, A., Alvear, M., Barrientos, L., & Salazar, L.A. (2015). Antibiofilm activity of Chilean propolis on Streptococcus mutans is influenced by the year of collection. BioMed Research International, 2015, 1–6.10.1155/2015/291351
  • Voigt, K., & Rademacher, E. (2015). Effect of the propolis components, cinnamic acid and pinocembrin, on Apis mellifera and Ascosphaera apis. Journal of Apicultural Science, 59, 89–95.
  • Williams, G.R., Sampson, A., Shutler, D., & Rogers, R.D. (2008). Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? Journal of Invertebrate Pathology, 99, 342–344.10.1016/j.jip.2008.04.005
  • Wilson, M.B., Brinkman, D., Spivak, M., Gardner, G., & Cohen, J.D. (2015). Regional variation in composition and antimicrobial activity of US propolis against Paenibacillus larvae and Ascosphaera apis. Journal of Invertebrate Pathology, 124, 44–50.10.1016/j.jip.2014.10.005
  • Yang, X., & Cox-Foster, D.L. (2005). Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proceedings of the National Academy of Sciences (PNAS), 21, 7470–7475.10.1073/pnas.0501860102
  • Yemor, T., Phiancharoen, M., & Benbow, E. (2015). Effects of stingless bee propolis on Nosema ceranae infected Asian honey bees, Apis cerana. Journal of Apicultural Research, 54(5), 468–473. doi: 10.1080/00218839.2016.1162447

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.