Accelerated Development and Toxin Tolerance of the Navel Orangeworm Amyelois transitella (Lepidoptera: Pyralidae) in the Presence of Aspergillus flavus

Abstract

The navel orangeworm (Amyelois transitella) and the fungus Aspergillus flavus constitute a facultative mutualism and pest complex in tree nut and fruit orchards in California. The possibility exists that the broad detoxification capabilities of A. flavus benefit its insect associate by metabolizing toxicants, including hostplant phytochemicals and pesticides. We 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 potato dextrose agar (PDA) diets and fed to larvae to evaluate the ability of the fungus to metabolize these chemicals. 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. Aspergillus 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 our findings, this mutualistic association should be considered in designing chemical management strategies for these pests.

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References

  1. (CDPR) California Department of Pesticide Regulation (2016) Pesticide use reporting. https://www.cdpr.ca.gov/docs/pur/pur16rep/16_pur.htm. Accessed August 2018

  2. Alvarenga N, Birolli WG, Seleghim MHR, Porto ALM (2014) Biodegradation of methyl parathion by whole cells of marine-derived fungi Aspergillus sydowii and Penicillium decaturense. Chemosphere 117:47–52

    CAS  Article  Google Scholar 

  3. Amaike S, Keller NP (2011) Aspergillus flavus. Annu Rev Phytopathol 49:107–133

    CAS  Article  Google Scholar 

  4. Ampt EA, Bush DS, Siegel JP, Berenbaum MR (2015) Larval preference and performance of Amyelois transitella (navel orangeworm, Lepidoptera: Pyralidae) in relation to the fungus Aspergillus flavus. Environ Entomol 45:155–162

    Article  Google Scholar 

  5. Bagchi VA, Siegel JP, Demkovich M, Zehr L, Berenbaum MR (2016) Impact of pesticide resistance on toxicity and tolerance of hostplant phytochemicals in Amyelois transitella (Lepidoptera: Pyralidae). J Insect Sci 16:1–7

    Article  Google Scholar 

  6. Beck JJ (2013) Conopthorin from almond host plant and fungal spores and its ecological relation to navel orangeworm: a natural products chemist’s perspective. J Mex Chem Soc 57:69–72

    CAS  Google Scholar 

  7. Berenbaum MR (1991a) Coumarins. In: Rosenthal G, Berenbaum M (eds) Herbivores: their interactions with secondary plant Metabolites, vol 1. Academic Press, New York, pp 221–249

    Google Scholar 

  8. Berenbaum MR (1991b) Comparative processing of allelochemicals in the Papilionidae (Lepidoptera). Arch Insect Biochem Physiol 17:213–222

    CAS  Article  Google Scholar 

  9. Bush DS, Lawrance A, Siegel JP, Berenbaum MR (2017) Orientation of navel orangeworm (Lepidoptera: Pyralidae) larvae and adults toward volatiles associated with almond hull split and Aspergillus flavus. Environ Entomol 46:602–608

    Article  Google Scholar 

  10. Campbell BC, Molyneux RJ, Schatzki TF (2003) Current research on reducing pre-and post-harvest aflatoxin contamination of US almond, pistachio, and walnut. Toxin Rev 22:225–266

    CAS  Google Scholar 

  11. Ceja-Navarro JA, Vega FE, Karaoz HUZ, Jenkins S, Lim HC, Kosina P, Infante F, Northen TR, Brodie EL (2015) Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat Commun 6:7618

    CAS  Article  Google Scholar 

  12. Connell JH (2002) Leading edge of plant protection for almond. Hort Technol 12:619–622

    Google Scholar 

  13. Cotty PJ (1994) Influence of field application of an atoxigenic strain of Aspergillus flavus on the populations of A. flavus infecting cotton bolls and on aflatoxin content of cottonseed. Phytopathol 84:1270–1277

    Article  Google Scholar 

  14. Cotty PJ, Bayman P (1993) Competitive exclusion of a toxigenic strain of Aspergillus flavus by an atoxigenic strain. Phytopathol 83:1283–1287

    Article  Google Scholar 

  15. Curtis RK, Barnes MM (1977) Oviposition and development of the navel orangeworm in relation to almond maturation. J Econ Entomol 70:395–398

    Article  Google Scholar 

  16. Demkovich M, Dana CE, Siegel JP, Berenbaum MR (2015a) Effect of piperonyl butoxide on the toxicity of four classes of insecticides to navel orangeworm (Amyelois transitella) (Lepidoptera: Pyralidae). J Econ Entomol 108:2753–2760

    Article  Google Scholar 

  17. Demkovich M, Siegel JP, Higbee BS, Berenbaum MR (2015b) Mechanism of resistance acquisition and potential associated fitness costs in Amyelois transitella (Lepidoptera: Pyralidae) exposed to pyrethroid insecticides. Environ Entomol 44:855–863

    Article  Google Scholar 

  18. Demkovich M, Siegel JP, Walse SS, Berenbaum MR (2018) Impact of agricultural adjuvants on the toxicity of the diamide insecticides chlorantraniliprole and flubendiamide on different life stages of the navel orangeworm (Amyelois transitella). J Pest Sci 91:1127–1136

    Article  Google Scholar 

  19. Desjardins AE, Spencer GF, Plattner RD, Beremand MN (1989) Furanocoumarin phytoalexins, trichothecene toxins, and infection of Pastinaca sativa by Fusarium sporotrichioides. Mol Plant Pathol 79:170–175

    CAS  Google Scholar 

  20. Doster MA, Michailides TJ (1994) The development of early split pistachio nuts and their contamination by molds, aflatoxins, and insects. Acta Hortic 419:359–364

    Google Scholar 

  21. Finney GL, Brinkman D (1967) Rearing the navel orangeworm in the laboratory. 1. J Econ Entomol 60:1109–1111

    Article  Google Scholar 

  22. Gilliam M, Prest DB, Morton HL (1974) Fungi isolated from honey bees, Apis mellifera, fed 2,4-D and antiobiotics. J Invertebr Pathol 21:213–217

    Article  Google Scholar 

  23. Gilliam M, Prest DB, Lorenz BJ (1989) Microbiology of pollen and bee bread: taxonomy and enzymology of molds. Apidologie 20:53–68

    Article  Google Scholar 

  24. Haviland DR, Symmes EJ, Adaskaveg JE, Duncan RA, Roncoroni JA, Gubler WD, Hanson B, Hembree KJ, Holtz BA, Stapleton JJ, Tollerup KE, Trouillas FP, Zalom FG (2017) UC IPM Pest Management Guidelines Almond. UC ANR Publication 3431. Oakland, CA

  25. Kele RA, McCoy E (1971) Defined liquid minimal medium for Caryophanon latum. Appl Microbiol 22:728–729

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Li X, Berenbaum MR, Schuler MA (2000) Molecular cloning and expression of CYP6B8: a xanthotoxin-inducible cytochrome P450 cDNA from Helicoverpa zea. Insect Biochem Mol Biol 30:75–84

    CAS  Article  Google Scholar 

  27. Liang WQ, Wang ZY, Li H, Wu PC, Hu JM, Luo N, Cao LX, Liu YH (2005) Purification and characterization of a novel pyrethroid hydrolase from Aspergillus niger ZD11. J Agric Food Chem 53:7415–7420

    CAS  Article  Google Scholar 

  28. Lund AE, Narahashi T (1983) Kinetics of sodium channel modification as the basis for the variation in the nerve membrane effects of pyrethroids and DDT analogs. Pestic Biochem Physiol 20:203–216

    CAS  Article  Google Scholar 

  29. Luo Y, Gao W, Doster M, Michailides T (2009) Quantification of conidial density of Aspergillus flavus and A. parasiticus in soil from almond orchards using real-time PCR. J Appl Microbiol 106:1649–1660

    CAS  Article  Google Scholar 

  30. Mao W, Berhow MA, Zangerl AR, McGovern J, Berenbaum MR (2006) Cytochrome P450-mediated metabolism of xanthotoxin by Papilio multicaudatus. J Chem Ecol 32:523–536

    CAS  Article  Google Scholar 

  31. Mukherjee I, Mittal A (2005) Bioremediation of endosulfan using Aspergillus terreus and Cladosporium oxysporum. Bull Environ Contam Toxicol 75:1034–1040

    CAS  Article  Google Scholar 

  32. Myung K, Manthey JA, Narciso JA (2008) Aspergillus niger metabolism of citrus furanocoumarin inhibitors of human cytochrome P450 3A4. Appl Microbiol Biotechnol 78:343–349

    CAS  Article  Google Scholar 

  33. Nigg HN, Nordby HE, Beier RC, Dillman A, Macias C, Hansen RC (1993) Phototoxic coumarins in limes. Food Chem Toxicol 31:331–335

    CAS  Article  Google Scholar 

  34. Niu G, Siegel J, Schuler MA, Berenbaum MR (2009) Comparative toxicity of mycotoxins to navel orangeworm (Amyelois transitella) and corn earworm (Helicoverpa zea). J Chem Ecol 35:951–957

    CAS  Article  Google Scholar 

  35. Niu G, Rupasingh SG, Zangerl AR, Siegel JP, Schuler MA, Berenbaum MR (2011) A substrate-specific cytochrome P450 monooxygenase, CYP6AB11, from the polyphagous navel orangeworm (Amyelois transitella). Insect Biochem Mol Biol 41:244–253

    CAS  Article  Google Scholar 

  36. Oliveira AP, Valentão P, Pereira JA, Silva BM, Tavares F, Andrad PB (2009) Ficus carica L.: metabolic and biological screening. Food Chem Toxicol 47:2841–2846

    CAS  Article  Google Scholar 

  37. Palumbo JD, Mahoney NE, Light DM, Siegel J, Puckett RD, Michailides TJ (2014) Spread of Aspergillus flavus by navel orangeworm (Amyelois transitella) on almond. Plant Dis 98:1194–1199

    Article  Google Scholar 

  38. Phillips D, Uota M, Monticelli D, Curtis C (1976) Colonization of almond by Aspergillus flavus. J Am Soc Hortic Sci 101:19–23

    Google Scholar 

  39. Ramadevi C, Nath MM, Prasad MG (2012) Mycodegradation of malathion by a soil fungal isolate, Aspergillus niger. Int J Basic Appl Chem Sci 2:108–115

    Google Scholar 

  40. Seyedmousavi S, Guillot J, Arné P, de Hoog GS, Mouton JW, Melchers WJG, Verweij PE (2015) Aspergillus and aspergilloses in wild and domestic animals: a global health concern with parallels to human disease. Med Mycol 53:765–797

    Article  Google Scholar 

  41. Teng WY, Huang YL, Huang RL, Chung RS, Chen CC (2004) Biotransformation of imperatorin by Aspergillus flavus. J Nat Prod 67:1014–1017

    CAS  Article  Google Scholar 

  42. USEPA (2017) Aspergillus flavus AF36; amendment to an exemption to a requirement of a tolerance. https://www.gpo.gov/fdsys/pkg/FR-2017-03-22/pdf/2017-05720.pdf

  43. Waldbauer G, Cohen RW, Friedman S (1984) Self-selection of an optimal nutrient mix from defined diets by larvae of the corn earworm, Heliothis zea (Boddie). Physiol Zool 57:590–597

    Article  Google Scholar 

  44. Watson GB (2001) Actions of insecticidal spinosyns on γ-aminobutyric acid responses from small-diameter cockroach neurons. Pestic Biochem Physiol 71:20–28

    CAS  Article  Google Scholar 

  45. Widstrom N (1979) The role of insects and other plant pests in aflatoxin contamination of corn, cotton, and peanuts—a review. J Environ Qual 8:5–11

    Article  Google Scholar 

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Acknowledgments

We thank Mark Demkovich for his advice and assistance. Daniel Raudabaugh advised us on mycology and experimental design, Dr. Rebecca Fuller advised us on graphing in R, and Dr. Themis Michailides provided the AF36 strain. This research was funded by the California Pistachio Research Board and the Almond Board of California. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture or the University of Illinois. USDA is an equal opportunity provider and employer.

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Correspondence to Daniel S. Bush.

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Bush, D.S., Siegel, J.P. & Berenbaum, M.R. Accelerated Development and Toxin Tolerance of the Navel Orangeworm Amyelois transitella (Lepidoptera: Pyralidae) in the Presence of Aspergillus flavus. J Chem Ecol 44, 1170–1177 (2018). https://doi.org/10.1007/s10886-018-1027-0

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Keywords

  • Navel orangeworm
  • Fungus
  • Pyrethroid
  • Spinosyn
  • Furanocoumarin
  • Detoxification