Fungal communities associated with almond throughout crop development: implications for aflatoxin biocontrol management in California

Authors: ORTEGA-BELTRAN, ALEJANDRO - University Of California, Davis; MORAL, JUAN - University Of California, Davis; PUCKETT, RYAN - University Of California, Davis; MORGAN, DAVID - University Of California, Davis; Cotty, Peter; MICHAILIDES, THEMIS - University Of California, Davis

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/3/2018
Publication Date: 6/20/2018
Citation: Ortega-Beltran, A., Moral, J., Puckett, R.D., Morgan, D.P., Cotty, P.J., Michailides, T.J. 2018. Fungal communities associated with almond throughout crop development: implications for aflatoxin biocontrol management in California. PLoS One. 13(6):e0199127. https://doi.org/10.1371/journal.pone.0199127.
DOI: https://doi.org/10.1371/journal.pone.0199127

Interpretive Summary: Aflatoxin producing fungi may contaminate almonds in California causing great reductions in the value of the crop. To prevent contamination, strains of Aspergillus flavus that do not utilize aflatoxins, called atoxigenic strains, are applied to orchards as biocontrol agents. Bees are required to pollinate almond. However, influences of Aspergillus flavus biocontrol treatments on bee health have not been explored. In order to evaluate potential impacts of seasonal dynamics of fungi and biocontrol applications on bees associated with almonds, populations of Aspergillus flavus associated with almond were monitored in blossoms and on the honey bees visiting blossoms over several years. In both blossoms and honey bees, A. flavus frequencies were low. And the A. flavus used for biocontrol of aflatoxins was very rare being detected only once. The evidence of low levels of the biocontrol atoxigenic strain of A. flavus on almond blossoms and bees during pollination of orchards treated with the biocontrol combined with the biocontrol agent’s effectiveness in limiting aflatoxin contamination in almond provide additional support for the registration of AF36 by USEPA for use in almond in California.

Technical Abstract: Interactions between pathogenic and nonpathogenic fungal species in the tree canopy are complex and can determine if disease will manifest in the plant and in other organisms such as honey bees. Seasonal dynamics of fungi were studied in an almond orchard in California where experimental release of the atoxigenic biopesticide Aspergillus flavus AF36 to displace toxigenic Aspergillus strains has been conducted for five years. The presence of the vegetative compatibility group (VCG) YV36, to which AF36 belongs, in the blossoms, and the honey bees that attend these blossoms, was assessed. In blossoms, A. flavus frequencies ranged from 0 to 4.5%, depending on the year of study. Frequencies of honey bees carrying A. flavus ranged from 6.5 to 10%. Only one A. flavus isolate recovered from a blossom in 2016 belonged to YV36, while members of the VCG were not detected contaminating honey bees. Exposure of pollinator honey bees to AF36 was detected to be very low. The density of several Aspergillus species was found to increase during almond hull split and throughout the final stages of maturation; this also occurred in pistachio orchards during the maturation period. Additionally, we found that AF36 effectively limited almond aflatoxin contamination in laboratory assays. This study provides knowledge and understanding of the seasonal dynamics of Aspergillus fungi and will help design aflatoxin management strategies for almond. The evidence of the low levels of VCG YV36 encountered on almond blossoms and bees during pollination and AF36’s effectiveness in limit aflatoxin contamination in almond provided additional support for the registration of AF36 with USEPA to use in almond in California.