Re-thinking management approaches in complex agroecosystems: relationships between the fungus Aspergillus flavus and two insects of economic importance

Bush, Daniel S

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https://hdl.handle.net/2142/117666 Copy

Description

Title

Re-thinking management approaches in complex agroecosystems: relationships between the fungus Aspergillus flavus and two insects of economic importance

Author(s)

Bush, Daniel S

Issue Date

2022-11-29

Director of Research (if dissertation) or Advisor (if thesis)

Berenbaum, May R

Doctoral Committee Chair(s)

Berenbaum, May R

Committee Member(s)

• Hanks, Lawrence
• Dolezal, Adam G
• Siegel, Joel P

Department of Study

Entomology

Discipline

Entomology

Degree Granting Institution

University of Illinois at Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

• navel orangeworm
• Aspergillus flavus
• insect-plant interactions
• insect-fungus interactions
• pyrethroids
• kaolin
• IPM
• Apis mellifera

Abstract

Insect-fungus interactions are common and, in many cases, well-studied. Leafcutter ants and bark beetles and their respective fungal associates have received attention, for instance. However, there is a vast variety of fungal pathogens that interact with insects of economic importance in ways and degrees that are as yet unknown. In particular, molds of the genera Aspergillus and Penicillium are nearly ubiquitous, and many species may infect an extensive list of potential hosts. They occur in all agricultural settings and thus encounter all manner of insect pests and pollinators. For instance, lepidopteran larvae and the phytopathogenic molds of the ascomycete fungi make up a disproportionate number of the major plant pests, yet relatively few studies exist concerning their effects on each other. I studied two insects of economic importance—the navel orangeworm and the Western honey bee—which are linked to each other by one highly opportunistic plant pathogen, Aspergillus flavus. A greater understanding of these relationships may shed light on the importance of fungal interactions with the plant enemies and plant mutualists that play critical roles in agroecosystems. The navel orangeworm Amyelois transitella (Walker) (Lepidoptera: Pyralidae) and the fungus Aspergillus flavus (Link) constitute a facultative mutualism and pest complex in tree nut and fruit orchards in California. Following on my previous work investigating nutritional benefits of this association, I posited that the broad detoxification capabilities of A. flavus might benefit its insect associate via metabolism of toxicants, including hostplant phytochemicals and pesticides. In Chapter 1, I examined this hypothesis by conducting laboratory bioassays to assess growth rates and survivorship of pyrethroid-resistant (R347) and susceptible (CPQ) larval strains on potato dextrose agar diet containing almond meal with and without two furanocoumarins, xanthotoxin and bergapten, found in several hostplants, and with and without two insecticides, bifenthrin and spinetoram, used in almond and pistachio orchards. Additionally, fungi were incubated in liquid diets containing the test chemicals, and extracts of these diets were added to almond PDA diets and fed to larvae to evaluate the ability of the fungus to metabolize these chemicals. I found that larvae consuming furanocoumarin-containing diet experienced higher mortality than individuals on unamended diets, but adding A. flavus resulted in up to 61.7% greater survival. A. flavus in the diet increased development rate > two-fold when furanocoumarins were present, demonstrating fungal enhancement of diet quality. Adding extracts of liquid diets containing xanthotoxin and fungus decreased mortality compared to xanthotoxin alone. On diets containing bifenthrin and spinetoram, however, mortality increased. These results support the hypothesis that A. flavus enhances navel orangeworm performance and contributes to detoxification of xenobiotics. Among practical implications of my findings, this mutualistic association should be considered in designing chemical management strategies for these pests. Toward this end, in Chapter 2 I examined the prevailing methods of control for navel orangeworm as well as possible alternatives. Contemporary production of almonds and pistachios in California's Central Valley requires the use of insecticides for the management of the navel orangeworm, the primary arthropod pest. The pyrethroid bifenthrin is commonly employed to control A. transitella, but a strain of A. transitella (R347) obtained from Kern County almond orchards with a history of heavy bifenthrin use has acquired resistance to pyrethroids. One method to restore efficacy of bifenthrin (or other primary insecticides that present a risk for resistance acquisition) is to use additives and spray adjuvants applied simultaneously to improve coverage and increase toxicity. I tested the naturally occurring clay kaolin as an additive to reduce A. transitella infestation of almonds and pistachios, administered alongside both bifenthrin and the diamide chlorantraniliprole. Larval performance was measured in laboratory studies for two strains of larvae, R347 and a pyrethroid-susceptible strain (ALM). The R347 larvae infested almonds in laboratory assays at higher rates, consistent with higher resistance or tolerance to both pesticide. The addition of kaolin reduced infestation levels and larval survival relative to each insecticide or kaolin alone; the survival of pyrethroid-resistant larvae on diet containing bifenthrin was significantly reduced. The increase in toxicity created by the addition of kaolin was confirmed in a field trial in pistachio orchards in the California Central Valley. These results suggest synergistic activity between kaolin and at least two insecticides and that adding kaolin to these two classes of insecticide may increase their efficacy and slow the evolution of insecticide resistance. Aspergillus fungi contribute to economic losses caused by navel orangeworm infestations. This fungus, which is ubiquitous and highly polyphagous, can be found throughout the almond agroecosystem, including within the hives of honey bees (Apis mellifera) brought into orchards during blooming periods to provide pollination services. Little is known about the role of this particular fungus in honey bee nutrition and success. Partly as a result of my prior work on insect-fungus mutualism, and partly because of recent evidence for the role of fungi and fungicides in apiculture, I hypothesized that the presence or absence of fungal species such as Aspergillus flavus could be an important part of the equation for global honey bee health. The honey bee endo- and ecto-microbiomes, including bacterial and fungal species, are known to be important in food preparation, processing, storage, and digestion. Aspergillus species are a disproportionately large part of the ectomicrobiome, which may indicate a role in contribute to the suitability of the honey bee’s primary food sources. However, conditions in the honey bee colony are frequently harsh for microbes and fungi such as A. flavus due in part to the xeric and acidic qualities of bee bread and the presence of propolis, a substance with antimicrobial properties. In Chapter 3, I used a variety of quantitative and qualitative assays to determine whether A. flavus isolated from Illinois bee hives shows signs of adaptation to hive conditions such as temperature, pH, osmotic pressure, and exposure to propolis. This comparison made use of three strains of A. flavus, including the experimental strain from Ch. 1-2 (AF36), a strain isolated from bee bread (AFBB), and another strain from a honey bee colony believed to be acutely pathogenic (AFPA). I found evidence that A. flavus found in bee bread is better able to tolerate some of these stresses than pathogenic and experimental strains. For instance, after several days of exposure to propolis, AFBB hyphal growth was far greater than that of AF36, and greater even than growth of AFPA by about one-third. Strain AFBB also withstood extremely acidic conditions significantly better than the other strains. These results may suggest a coevolutionary relationship between certain fungal strains and honey bees. Aspergillus flavus plays an unpredictable role in insect-fungus interactions and agroecosystems, and as widespread and economically important as this fungus is, it is useful to gain a better understanding of what conditions govern its pathogenicity or domestication.

Graduation Semester

2022-12

Type of Resource

Thesis

Copyright and License Information

Copyright 2022 Daniel Bush

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