Compatibility of Metarhizium anisopliae and Beauveria bassiana with insecticides and fungicides used in macadamia production in Australia

Article

Khun, Kim Khuy, Ash, Gavin J., Stevens, Mark M., Huwer, Ruth K. and Wilson, Bree A.L.. 2021. "Compatibility of Metarhizium anisopliae and Beauveria bassiana with insecticides and fungicides used in macadamia production in Australia." Pest Management Science. 77 (2), pp. 709-718. https://doi.org/10.1002/ps.6065
Article Title

Compatibility of Metarhizium anisopliae and Beauveria bassiana with insecticides and fungicides used in macadamia production in Australia

ERA Journal ID5321
Article CategoryArticle
AuthorsKhun, Kim Khuy (Author), Ash, Gavin J. (Author), Stevens, Mark M. (Author), Huwer, Ruth K. (Author) and Wilson, Bree A.L. (Author)
Journal TitlePest Management Science
Journal Citation77 (2), pp. 709-718
Number of Pages10
Year2021
PublisherJohn Wiley & Sons
Place of PublicationUnited Kingdom
ISSN1526-498X
1526-4998
Digital Object Identifier (DOI)https://doi.org/10.1002/ps.6065
Web Address (URL)https://onlinelibrary.wiley.com/doi/abs/10.1002/ps.6065
Abstract

Background
Integrating fungal biocontrol agents into crop protection programs dominated by synthetic pesticides is an important first step towards developing an IPM program, however their successful integration relies on an understanding of how their performance may be impacted by the remaining agrochemicals deployed for managing other pests and diseases. In this study we tested ten formulated pesticides used in macadamia production at different concentrations to determine their effects on the germination, mycelial growth and sporulation of Metarhizium anisopliae and Beauveria bassiana in vitro. Further tests with laboratory grade actives of the non‐compatible pesticides were conducted to determine whether any antagonistic effects were caused by the active constituent or by formulation additives.

Results
At their registered concentrations, formulated trichlorfon, acephate and indoxacarb were compatible with M. anisopliae, whereas B. bassiana showed compatibility with formulated trichlorfon, acephate, indoxacarb, sulfoxaflor and spinetoram. Bioassays using laboratory grade active constituents indicated that the adverse impact of formulated beta‐cyfluthrin on both fungal species and that of formulated methidathion on B. bassiana is probably due to components of the emulsifiable concentrate formulations rather than their active constituents. Diazinon was the only insecticidal active that showed high toxicity to both fungal species. The two fungicides, carbendazim and pyraclostrobin, were toxic to both fungal species at all tested concentrations.

Conclusion
Our results identify which pesticides used on macadamias in Australia are compatible and incompatible with entomopathogenic fungi. Future studies on pesticides degradation rates will help define the spray intervals required to eliminate these adverse effects.

Keywordsbiological index, compatibility, entomopathogenic fungi, fungicides, insecticides
ANZSRC Field of Research 2020300210. Sustainable agricultural development
300804. Horticultural crop protection (incl. pests, diseases and weeds)
Byline AffiliationsCentre for Crop Health
Department of Primary Industries, New South Wales
Institution of OriginUniversity of Southern Queensland
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Wilson, B. A. L., Ash, G. J. and Harper, J. D. I.. 2012. "Arbuscular mycorrhizal fungi improve the growth and nodulation of the annual legume messina (Melilotus siculus) under saline and non-saline conditions." Crop and Pasture Science. 63 (2), pp. 164-178. https://doi.org/10.1071/CP11193
The effects of defoliation on plant community, root biomass and nutrient allocation and soil chemical properties on semi-arid steppes in northern China
Guo, Y-J., Han, L., Li, G-D., Han, J-G., Wang, G-L., Li, Z-Y. and Wilson, B.. 2012. "The effects of defoliation on plant community, root biomass and nutrient allocation and soil chemical properties on semi-arid steppes in northern China." Journal of Arid Environments. 78, pp. 128-134. https://doi.org/10.1016/j.jaridenv.2011.11.003
Plant-parasitic nematodes as invasive species: Characteristics, uncertainty and biosecurity implications
Singh, S. K., Hodda, M., Ash, G. J. and Banks, N. C.. 2013. "Plant-parasitic nematodes as invasive species: Characteristics, uncertainty and biosecurity implications." Annals of Applied Biology. 163 (3), pp. 323-350. https://doi.org/10.1111/aab.12065
Bacteria associated with sheath browning and grain discoloration of rice in East Timor and implications for Australia’s biosecurity
Adorada, Dante L., Stodart, Benjamin J., Tpoi, Roni P., Costa, Severino S. and Ash, Gavin J.. 2013. "Bacteria associated with sheath browning and grain discoloration of rice in East Timor and implications for Australia’s biosecurity." Australasian Plant Disease Notes. 8 (1), pp. 43-47. https://doi.org/10.1007/s13314-013-0092-z
Development of a genomics-based LAMP (loop-mediated isothermal amplification) assay for detection of Pseudomonas fuscovaginae from rice
Ash, Gavin J., Lang, Jillian M., Triplett, Lindsay R., Stodart, Benjamin J., Verdier, Valerie, Vera Cruz, Casiana, Rott, Philippe and Leach, Jan E.. 2014. "Development of a genomics-based LAMP (loop-mediated isothermal amplification) assay for detection of Pseudomonas fuscovaginae from rice ." Plant Disease: an international journal of applied plant pathology. 98 (7), pp. 909-915. https://doi.org/10.1094/PDIS-09-13-0957-RE
Identification of virulence associated loci in the emerging broad host range plant pathogen Pseudomonas fuscovaginae
Patel, Hitendra Kumar, Matiuzzo, Maura, Bertani, Iris, Bigirimana, Vincent De Paul, Ash, Gavin J., Hofte, Monica and Venturi, Vittoria. 2014. "Identification of virulence associated loci in the emerging broad host range plant pathogen Pseudomonas fuscovaginae." BMC Microbiology. 14 (274), pp. 1-13. https://doi.org/10.1186/s12866-014-0274-7
Identification of QTLs associated with resistance to phomopsis pod blight (Diaporthe toxica) in Lupinus albus
Cowley, Raymond, Luckett, David J., Ash, Gavin J., Harper, John D. I., Vipin, Cina A., Raman, Harsh and Ellwood, Simon. 2014. "Identification of QTLs associated with resistance to phomopsis pod blight (Diaporthe toxica) in Lupinus albus." Breeding Science. 64 (1), pp. 83-89. https://doi.org/10.1270/jsbbs.64.83
Prioritising plant-parasitic nematode species biosecurity risks using self organising maps
Singh, Sunil K., Paini, Dean R., Ash, Gavin J. and Hodda, Mike. 2014. "Prioritising plant-parasitic nematode species biosecurity risks using self organising maps." Biological Invasions. 16 (7), pp. 1515-1530. https://doi.org/10.1007/s10530-013-0588-7
Responses of physiological indexes and leaf epicuticular waxes of Brassica napus to Sclerotinia sclerotiorum infection
Ni, Y., Guo, Y. -J., Wang, J., Xia, R. -E., Wang, X. -Q., Ash, G. and Li, J. -N.. 2014. "Responses of physiological indexes and leaf epicuticular waxes of Brassica napus to Sclerotinia sclerotiorum infection." Plant Pathology. 63 (1), pp. 174-184. https://doi.org/10.1111/ppa.12060
The genome sequence of the biocontrol fungus Metarhizium anisopliae and comparative genomics of Metarhizium species
Pattemore, Julie A., Hane, James K., Williams, Angela H., Wilson, Bree A. L., Stodart, Ben J. and Ash, Gavin J.. 2014. "The genome sequence of the biocontrol fungus Metarhizium anisopliae and comparative genomics of Metarhizium species." BMC Genomics. 15 (1), pp. 1-15. https://doi.org/10.1186/1471-2164-15-660
Keeping ‘one step ahead’ of invasive species: using an integrated framework to screen and target species for detailed biosecurity risk assessment
Singh, Sunil K., Ash, Gavin J. and Hodda, Mike. 2015. "Keeping ‘one step ahead’ of invasive species: using an integrated framework to screen and target species for detailed biosecurity risk assessment." Biological Invasions. 17 (4), pp. 1069-1086. https://doi.org/10.1007/s10530-014-0776-0
Implications of bacterial contaminated seed lots and endophytic colonization by Pseudomonas fuscovaginae on rice establishment
Adorada, D. L., Stodart, B. J., Pangga, I. B. and Ash, G. J.. 2015. "Implications of bacterial contaminated seed lots and endophytic colonization by Pseudomonas fuscovaginae on rice establishment." Plant Pathology. 64 (1), pp. 43-50. https://doi.org/10.1111/ppa.12243
Hierarchical genetic variation of Botryosphaeriaceae species associated with decline and dieback of grapevine in south-eastern Australia
Qui, Y., Steel, C. C., Ash, G. J. and Savocchia, S.. 2015. "Hierarchical genetic variation of Botryosphaeriaceae species associated with decline and dieback of grapevine in south-eastern Australia." Australian Journal of Grape and Wine Research. 21 (3), pp. 458-467. https://doi.org/10.1111/ajgw.12144
Gulypyrones A and B and Phomentrioloxins B and C Produced by Diaporthe gulyae, a Potential Mycoherbicide for Saffron Thistle (Carthamus lanatus)
Andolfi, Anna, Boari, Angela, Evidente, Marco, Cimmino, Alessio, Vurro, Maurizio, Ash, Gavin and Evidente, Antonio. 2015. "Gulypyrones A and B and Phomentrioloxins B and C Produced by Diaporthe gulyae, a Potential Mycoherbicide for Saffron Thistle (Carthamus lanatus)." Journal of Natural Products. 78 (4), pp. 623-629. https://doi.org/10.1021/np500570h
Structure and Absolute Configuration of Kongiidiazadione, a NewPhytotoxic 3-Substituted-5-Diazenylcyclopentendione Produced by Diaporthe Kongii
Evidente, Marco, Boari, Angela, Vergura, Stefania, Cimmino, Alessio, Vurro, Maurizio, Ash, Gavin, Superchi, Stefano and Evidente, Antonio. 2015. "Structure and Absolute Configuration of Kongiidiazadione, a NewPhytotoxic 3-Substituted-5-Diazenylcyclopentendione Produced by Diaporthe Kongii." Chirality: the pharmacological, biological, and chemical consequences of molecular asymmetry. 27 (9), pp. 557-562. https://doi.org/10.1002/chir.22466
Whole genome phylogeny of Bacillus by feature frequency profiles (FFP)
Wang, Aisuo and Ash, Gavin J.. 2015. "Whole genome phylogeny of Bacillus by feature frequency profiles (FFP)." Scientific Reports. 5, pp. 1-14. https://doi.org/10.1038/srep13644
Biological control of sclerotinia stem rot of canola using antagonistic bacteria
Kamal, M. M., Lindbeck, K. D., Savocchia, S. and Ash, G. J.. 2015. "Biological control of sclerotinia stem rot of canola using antagonistic bacteria ." Plant Pathology. 64 (6), pp. 1375-1384. https://doi.org/10.1111/ppa.12369
Biology and biocontrol of Sclerotinia sclerotiorum (Lib.) de Bary in oilseed Brassicas
Kamal, Mohd. Mostofa, Savocchia, Sandra, Lindbeck, Kurt D. and Ash, Gavin J.. 2016. "Biology and biocontrol of Sclerotinia sclerotiorum (Lib.) de Bary in oilseed Brassicas." Australasian Plant Pathology. 45 (1), pp. 1-14. https://doi.org/10.1007/s13313-015-0391-2
Loop-mediated isothermal amplification for the detection of Pseudomonas fuscovaginae
Ash, G. J., Lang, J. M., Triplett, L. R., Stodart, B. J., Verdier, V. and Leach, J. E.. 2013. "Loop-mediated isothermal amplification for the detection of Pseudomonas fuscovaginae." 2013 APS-MSA Joint Meeting. United States 10 - 14 Aug 2013 United States. American Phytopathological Society.
Phomentrioloxin: A Phytotoxic Pentasubstituted Geranylcyclohexentriol Produced by Phomopsis sp., a Potential Mycoherbicide for Carthamus lanatus Biocontrol
Cimmino, Alessio, Andolfi, Anna, Zonno, Maria C., Troise, Ciro, Santini, Antonello, Tuzi, Angela, Vurro, Maurizio, Ash, Gavin and Evidente, Antonio. 2012. "Phomentrioloxin: A Phytotoxic Pentasubstituted Geranylcyclohexentriol Produced by Phomopsis sp., a Potential Mycoherbicide for Carthamus lanatus Biocontrol." Journal of Natural Products. 75 (6), pp. 1130-1137. https://doi.org/10.1021/np300200j
The science, art and business of successful bioherbicides
Ash, G. J.. 2010. "The science, art and business of successful bioherbicides." Biological Control. 52 (3), pp. 230-240. https://doi.org/10.1016/j.biocontrol.2009.08.007
The characterization and diversity of bacterial endophytes of grapevine
West, E. R., Cother, E. J., Steel, C. C. and Ash, G. J.. 2010. "The characterization and diversity of bacterial endophytes of grapevine." Canadian Journal of Microbiology. 56 (3), pp. 209-216. https://doi.org/10.1139/W10-004
Australia and New Zealand biocontrol conference: Emerging themes, future prospects
Gurr, Geoff M.., Horne, Paul, Page, Jessica, Ash, Gavin J. and Pilkington, Leigh J.. 2010. "Australia and New Zealand biocontrol conference: Emerging themes, future prospects." Biological Control. 52 (3), pp. 195-197. https://doi.org/10.1016/j.biocontrol.2010.01.001
Genotypic analysis of Mucor from the platypus in Australia
Connolly, J. H., Stodart, B. J. and Ash, G. J.. 2010. "Genotypic analysis of Mucor from the platypus in Australia." Journal of Wildlife Diseases. 46 (1), pp. 55-69. https://doi.org/10.7589/0090-3558-46.1.55
Development of strain specific molecular markers for the Sclerotinia minor bioherbicide strain IMI 344141
Pan, L., Ash, G. J., Ahn, B. and Watson, A. K.. 2010. "Development of strain specific molecular markers for the Sclerotinia minor bioherbicide strain IMI 344141." Biocontrol Science and Technology. 20 (9), pp. 939-959. https://doi.org/10.1080/09583157.2010.491895
Evidence that Diaporthe toxica infection of Lupinus albus is an emerging concern for the Australian lupin industry
Cowley, R. B., Ash, G. J., Harper, J. D. I. and Luckett, D. J.. 2010. "Evidence that Diaporthe toxica infection of Lupinus albus is an emerging concern for the Australian lupin industry." Australasian Plant Pathology. 39 (2), pp. 146-153. https://doi.org/10.1071/AP09067
Physiological characterization of the dandelion bioherbicide, Sclerotinia minor IMI 344141
Shaheen, In'aam Y., Abu-Dieyeh, Mohammed H., Ash, Gavin J. and Watson, Alan K.. 2010. "Physiological characterization of the dandelion bioherbicide, Sclerotinia minor IMI 344141." Biocontrol Science and Technology. 20 (1), pp. 57-76. https://doi.org/10.1080/09583150903419520
Influence of cultural and environmental conditions on conidial production, conidial germination and infectivity of Rhynchosporium alismatis, a candidate mycoherbicide
Jahromi, F. G., Ash, G. J. and Cother, E. J.. 1998. "Influence of cultural and environmental conditions on conidial production, conidial germination and infectivity of Rhynchosporium alismatis, a candidate mycoherbicide." Australasian Plant Pathology. 27 (3), pp. 180-185. https://doi.org/10.1071/AP98020
Suppressive effects of Rhynchosporium alismatis on different growth stages of Damasonium minus
Jahromi, F. G., Ash, G. J., Cother, E. J. and SOC ESPANOLA MALHERBOLOGIA. 1997. "Suppressive effects of Rhynchosporium alismatis on different growth stages of Damasonium minus." 1997 Congress of the Sociedad-Espanola-de-Malherbologia. Spain 24 - 26 Nov 1997 Spain.
Phomopsis spp. associated with die-back of saffron thistle (Carthamus lanatus)
Crump, N. S., Ash, G. J. and Nikandrow, A.. 1996. "Phomopsis spp. associated with die-back of saffron thistle (Carthamus lanatus)." Australasian Plant Pathology. 25 (2), p. 143. https://doi.org/10.1071/AP96025
Effect of Post-Inoculation Temperature and Light Intensity on Expression of Resistance to Stripe Rust in Some Australian Wheat Cultivars
Ash, G. J. and Rees, R. G.. 1994. "Effect of Post-Inoculation Temperature and Light Intensity on Expression of Resistance to Stripe Rust in Some Australian Wheat Cultivars." Australian Journal of Agricultural Research. 45 (7), pp. 1379-1386. https://doi.org/10.1071/AR9941379
Effects of temperature on the response of some Australian wheat cultivars to Puccinia striiformis f. sp. tritici
Park, Robert F., Ash, Gavin J. and Rees, Robert G.. 1992. "Effects of temperature on the response of some Australian wheat cultivars to Puccinia striiformis f. sp. tritici." Mycological Research. 96 (3), pp. 166-170. https://doi.org/10.1016/S0953-7562(09)80961-1
Yield losses in wheat caused by stripe rust (Puccinia striiformis West.) in northern New South Wales
Ash, G J.. and Brown, J. F.. 1990. "Yield losses in wheat caused by stripe rust (Puccinia striiformis West.) in northern New South Wales." Australian Journal of Experimental Agriculture. 30 (1), pp. 103-108. https://doi.org/10.1071/EA9900103