Pathogenicity bioassays of Ascosphaera apis strains from Spanish provinces in bee larvae from Northern Argentina

References

• Abrol, D. P., Gorka, A. K., Ansari, M. J., Al-Ghamdi, A., & Al-Kahtani, S. (2019). Impact of insect pollinators on yield and fruit quality of strawberry. Saudi Journal of Biological Sciences, 26(3), 524–530. https://doi.org/10.1016/j.sjbs.2017.08.003
   PubMed Web of Science ®Google Scholar
• Ahmed, A. (2008). Manual Apícola del Norte Argentino. Magna.
   Google Scholar
• Albo, G., Córdoba, S., & Reynaldi, F. (2017). Chalkbrood: Pathogenesis and the interaction with honeybee defenses. International Journal of Environmental & Agriculture Research, 3(1), 71–80.
   Google Scholar
• Alonso, J. M., Rey, J., Puerta, F., Hermoso de Mendoza, J., Hermoso de Mendoza, M., & Flores, J. M. (1993). Enzymatic equipmet of Ascosphaera apis and the development of infection by this fungus in Apis mellifera. Apidologie, 24(4), 383–390. https://doi.org/10.1051/apido:19930404
   Web of Science ®Google Scholar
• Álvarez-Ramírez, A., Jiménez-González, L., Ortiz-Muñoz, E., Ruíz-García, I., & Orozco-Hernández, R. (2017). Influencia de las condiciones ambientales en la presentación de Ascosferosis (Ascosphaera apis) o cría de cal en Apis mellifera (abeja). Abanico Veterinario, 7(3), 37–46. https://doi.org/10.21929/abavet2017.73.4
   Google Scholar
• Ansari, M. J., Al-Ghamdi, A., Usmani, S., Khan, K. A., Alqarni, A. S., Kaur, M., & Al-Waili, N. (2017). In vitro evaluation of the effects of some plant essential oils on Ascosphaera apis, the causative agent of Chalkbrood disease. Saudi Journal of Biological Sciences, 24(5), 1001–1006. https://doi.org/10.1016/j.sjbs.2016.04.016
   PubMed Web of Science ®Google Scholar
• Aronstein, K., & Murray, K. D. (2010). Chalkbrood disease in honey bees. Journal of Invertebrate Pathology, 103(1), S20–S29. https://doi.org/10.1016/j.jip.2009.06.018
   PubMedGoogle Scholar
• Audisio, M. C., & Benítez-Ahrendts, M. R. (2011). Lactobacillus johnsonii CRL1647, isolated from Apis mellifera L. bee-gut, exhibited a beneficial effect on honeybee colonies. Beneficial Microbes, 2(1), 29–34. https://doi.org/10.3920/BM2010.0024
   PubMed Web of Science ®Google Scholar
• Benitez-Ahrendts, M. R., Tejerina, M. R., & Gutierrez Agüero, J. A. (2017). Selección de reinas de Apis mellifera de ecotipo local (provincia de Jujuy) tolerantes a Varroa sp. con alto nivel productivo de miel. In Libro de Resúmenes de las X Jornadas Científico- Técnicas de la Facultad de Ciencias Agrarias, 25–32. UNJU.
   Google Scholar
• Chen, D., Guo, R., Xiong, C., Zheng, Y., Hou, C., & Fu, Z. (2018). Morphological and molecular identification of chalkbrood disease pathogen Ascosphaera apis in Apis cerana cerana. Journal of Apicultural Research, 57(4), 516–521. https://doi.org/10.1080/00218839.2018.1475943
   Web of Science ®Google Scholar
• Cornman, R. S., Bennett, A. K., Murray, K. D., Evans, J. D., Elsik, C. G., & Aronstein, K. (2012). Transcriptome analysis of the honey bee fungal pathogen, Ascosphaera apis: Implications for host pathogenesis. BMC Genomics, 13, 285 https://doi.org/10.1186/1471-2164-13-285
   PubMed Web of Science ®Google Scholar
• DeGrandi-Hoffman, G., & Chen, Y. (2015). Nutrition, immunity and viral infections in honey bees. Current Opinion in Insect Science, 10, 170–176. https://doi.org/10.1016/j.cois.2015.05.007
   PubMed Web of Science ®Google Scholar
• Di Rienzo, J. A., Casanoves, F., Balzanini, M. G., Gonzalez, L., Tablada, M., & Robledo, C. W. (2008). Grupo Infostat, versión 2008. FCA, Univ. Nacional de Córdoba.
   Google Scholar
• Diao, Q., Yang, D., Zhao, H., Deng, S., Wang, X., Hou, C., & Wilfert, L. (2019). Prevalence and population genetics of the emerging honey bee pathogen DWV in Chinese apiculture. Scientific Reports, 9(1), 1–10. https://doi.org/10.1038/s41598-019-48618-y
   Google Scholar
• Evans, J. D., Aronstein, K., Chen, Y. P., Hetru, C., Imler, J.-L., Jiang, H., Kanost, M., Thompson, G. J., Zou, Z., & Hultmark, D. (2006). Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology, 15(5), 645–656. https://doi.org/10.1111/j.1365-2583.2006.00682.x
   PubMed Web of Science ®Google Scholar
• Flores, J. M., Gutiérrez, I., & Puerta, F. (2004). A comparison of methods to experimentally induce chalkbrood disease in honey bees. Spanish Journal of Agricultural Research, 2(1), 79–83. https://doi.org/10.5424/sjar/2004021-63
   Google Scholar
• Flores, J. M., Ruiz, J. A., Ruz, J. M., Puerta, F., Busto, M., Padilla, F., & Campano, F. (1996). Effect of temperature and humidity of sealed brood on chalkbrood development under controlled conditions. Apidologie, 27(4), 185–192. https://doi.org/10.1051/apido:19960401
   Web of Science ®Google Scholar
• Getachew, A., Wubie, A. J., Wu, J., Xu, J., Wu, P., Abejew, T. A., Tu, Y., Zhou, T., & Xu, S. F. (2018). Molecular identification of pathogenicity associated genes in honeybee fungal pathogen, Ascosphaera apis, by restricted enzyme-mediated integration (REMI) constructed mutants. International Journal of Agriculture and Biology, 20, 2879–2890.
   Web of Science ®Google Scholar
• Giacobino, A., Pacini, A., Molineri, A., Rodríguez, G., Crisanti, P., Bulacio Cagnolo, N., Merke, J., Orellano, E., Bertozzi, E., Pietronave, H., & Signorini, M. (2018). Potential associations between the mite Varroa destructor and other stressors in honeybee colonies (Apis mellifera L.) in temperate and subtropical climate from Argentina. Preventive Veterinary Medicine, 159, 143–152. https://doi.org/10.1016/j.prevetmed.2018.09.011
   PubMed Web of Science ®Google Scholar
• Hillyer, J. F. (2016). Insect immunology and hematopoiesis. Developmental and Comparative Immunology, 58, 102–118. https://doi.org/10.1016/j.dci.2015.12.006
   PubMed Web of Science ®Google Scholar
• Hystad, E. M., Salmela, H., Amdam, G. V., & Munch, D. (2017). Hemocyte-mediated phagocytosis differs between honey bee (Apis mellifera) worker castes. PLoS One, 12(9), e0184108. https://doi.org/10.1371/journal.pone.0184108
   PubMed Web of Science ®Google Scholar
• Invernizzi, C. (2001). Resistencia a la enfermedad de cría yesificada por colonias de Apis mellifera con eficiente comportamiento higiénico (Hymenoptera, Apidae). Iheringia. Série Zoologia, (91), 108–114. https://doi.org/10.1590/S0073-47212001000200016
   Google Scholar
• Jensen, A. B., Aronstein, K., Flores, J. M., Vojvodic, S., Palacio, M. A., & Spivak, M. (2013). Standard methods for fungal brood disease research. Journal of Apicultural Research, 52(1), 1–20. https://doi.org/10.3896/IBRA.1.52.1.13
   Web of Science ®Google Scholar
• Klinger, E. G., James, R. R., Youssef, N. N., & Welker, D. L. (2013). A multi-gene phylogeny provides additional insight into the relationships between several Ascosphaera species. J Invertebr Pathol, 112(1), 41–48. https://doi.org/10.1016/j.jip.2012.10.011
   PubMed Web of Science ®Google Scholar
• Lundgren, J., & Jurat-Fuentes, J. L. (2012). Physiology and ecology of host defense against microbial invaders. In: H. Kaya & F. Vega (Eds.), Insect pathology (pp. 461–480). 2nd Ed. University of Tennessee. Elsevier. https://doi.org/10.1016/b978-0-12-384984-7.00013-0
   Google Scholar
• Maxfield-Taylor, S. A., Mujic, A. B., & Rao, S. (2015). First detection of the larval chalkbrood disease pathogen Ascosphaera apis (Ascomycota: Eurotiomycetes: Ascosphaerales) in adult bumble bees. PLoS One, 10(4), e0124868. https://doi.org/10.1371/journal.pone.0124868
   PubMed Web of Science ®Google Scholar
• Moretto, G., Guerra, J. C., & Bittencourt, C. V. (2006). Uncapping activity of Apis mellifera L. (Hymenoptera: Apidae) towards worker brood cells infested with the mite Varroa destructor Anderson & Treuman (Mesostigmata: Varroidae). Neotropical Entomology, 35(3), 299–301. https://doi.org/10.1590/s1519-566x2006000300002
   PubMed Web of Science ®Google Scholar
• Novicov-Fanciotti, M., Tejerina, M., Benítez-Ahrendts, M. R., & Audisio, M. C. (2017). Honey yield of different commercial apiaries treated with Lactobacillus salivarius A3iob, a new bee-probiotic strain Beneficial Microbes, 9(2), 291–298. https://doi.org/10.3920/BM2017.0089
   PubMed Web of Science ®Google Scholar
• Ollerton, J., Winfree, R., & Tarrant, S. (2011). How many flowering plants are pollinated by animals? Oikos, 120(3), 321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
   Web of Science ®Google Scholar
• Padilla, F., Flores, J. M., & Campano, F. (2014). Control de la ascosferosis (Ascosphaera apis) mediante el uso de fondos higiénicos de rejilla. Actas Iberoamericanas de Conservación Animal (AICA), 4, 289–291.
   Google Scholar
• Pacini, A., Mira, A., Molineri, A., Giacobino, A., Bulacio Cagnolo, N., Aignasse, A., Zago, L., Izaguirre, M., Merke, J., Orellano, E., Bertozzi, E., Pietronave, H., Russo, R., Scannapieco, A., Lanzavecchia, S., Schnittger, L., Signorini, M., et. al. (2016). Distribution and prevalence of Nosema apis and N. ceranae in temperate and subtropical eco-regions of Argentina. Journal of Invertebrate Pathology, 141, 34–37. https://doi.org/10.1016/j.jip.2016.11.002
   PubMed Web of Science ®Google Scholar
• Palacio, M. A., Rodriguez, E., Goncalves, L., Bedascarrasbure, E., & Spivak, M. (2010). Hygienic behaviours of honey bees in response to brood experimentally pin-killed or infected with Ascosphaera apis. Apidologie, 41(6), 602–612. https://doi.org/10.1051/apido/2010022
   Web of Science ®Google Scholar
• Pereira, K. S., Meeus, I., & Smagghe, G. (2019). Honey bee-collected pollen is a potential source of Ascosphaera apis infection in managed bumble bees. Scientific Reports, 9(1), 4241 https://doi.org/10.1038/s41598-019-40804-2
   PubMed Web of Science ®Google Scholar
• Porrini, L. P., Quintana, S., Brasesco, C., Porrini, M. P., Garrido, P. M., Eguaras, M. J., Müller, F., & Fernandez Iriarte, P. (2020). Southern limit of africanized honey bee in Argentina. Journal of Apicultural Research, 59(4), 648–657. https://doi.org/10.1080/00218839.2019.1681116
   Web of Science ®Google Scholar
• Principal, J., D'Aubeterre, Barrios, R., Carlos, P. C., García de la Rosa, S., & Fuselli, S. R. (2008). Hygienic behavior of africanized honeybees (Apis mellífera Scutellata Lepeletier) in apiaries of Lara State. Venezuela. Zootecnia Tropical, 26(2), 167–173.
   Google Scholar
• Reynaldi, F. J., López, A. C., Albo, G. N., & Alippi, A. M. (2003). Differentiation of Ascosphaera apis isolates by rep-PCR fingerprinting and determination of chalkbrood incidence in Argentinean honey samples. Journal of Apicultural Research, 42(4), 68–76. https://doi.org/10.1080/00218839.2003.11101096
   Web of Science ®Google Scholar
• Reynaldi, F. J., Lucia, M., & Garcia Genchi, M. L. (2015). Ascosphaera apis, the entomopathogenic fungus affecting larvae of native bees (Xylocopa augusti): First Report in South America. Revista Iberoamericana de Micologia, 32(4), 261–264. https://doi.org/10.1016/j.riam.2015.01.001
   PubMed Web of Science ®Google Scholar
• Sanchez, C., Castignani, H., & Rabaglio, M. (2018). Mercado apícola internacional. PNAPI 1112052-Gestión de la innovación como Aporte para el Desarrollo Territorial. Instituto Nacional de Tecnología Agropecuaria. http://hdl.handle.net/20.500.12123/3063
   Google Scholar
• Siva-Jothy, M. T., Moret, Y., & Rolff, J. (2005). Insect immunity: An evolutionary ecology perspective. Advances in Insect Physiology, 32, 1–48. https://doi.org/10.1016/s0065-2806(05)32001-7
   Web of Science ®Google Scholar
• Takatori, K., & Tanaka, I. (1982). Ascosphaera apis isolated from chalkbrood in honey bees. Nihon Chikusan Gakkaiho , 53(2), 89–92. https://doi.org/10.2508/chikusan.53.89
   Google Scholar
• Tejerina, M. R., Cabana, M. J., Carrillo, L., & Benitez Ahrendts, M. R. (2018). Effect of Lactic Bacteria on Ascosphaera apis and A. atra. Asian Journal of Agriculture and Food Sciences, 6(4), 123–128. https://doi.org/10.24203/ajafs.v6i4.5405
   Google Scholar
• Tejerina, M. R., Cabana, M. J., Flores, J. M., & Benítez-Ahrendts, M. R. (2019). Studies of Ascosphaera apis strains isolated from commercial pollens of different Spanish provinces and their enzymatic production capacity. Archivos de Zootecnia, 68(263), 324–330. https://doi.org/10.21071/az.v68i263.4189
   Google Scholar
• Tejerina, M. R., Benítez-Ahrendts, M. R., & Audisio, M. C. (2020). Lactobacillus salivarius A3iob reduces the incidence of varroa destructor and Nosema Spp. in commercial apiaries located in the Northwest of Argentina. Probiotics and Antimicrobial Proteins, 12(4), 1360–1369. https://doi.org/10.1007/s12602-020-09638-7
   PubMedGoogle Scholar
• Wynns, A. A. (2012). The bee specialist fungus family Ascosphaeraceae and its allies: Systematics [ecology and co-evolution with solitary bees. [Ph.D. thesis]. Department of Agriculture and Ecology, University of Copenhagen.
   Google Scholar