Abstract
The study aims to determine the timing of application for high efficacy of Metarhizium anisopliae as a biocontrol agent. A field experiment was undertaken with M. anisopliae applied to the soil at five intervals during the peanut crop lifecycle, at seed germination (day 0) through to pod filling period [75 days after sowing (DAS)], and assessed the change of M. anisopliae density by sampling rhizospheric soil, subsequently at regular intervals and testing counts (CFU/g dry soil) through to harvest. The crop was sown into soil with an established white grub population, with larval density determined at harvest when the trial was concluded. Applications at 0, 15 and 30 days in the crop growth cycle, saw M. anisopliae mean propagule counts drop significantly after 15 days before increasing over the following 15–45 days. We observed an elevated mean increase in counts 30–45 days after application at the early flowering stage (30 DAS). Irrespective of application timing, in general, M. anisopliae densities declined to less than the initial 10% in the late stages of peanut development. At harvest, larval densities in all M. anisopliae treatments were significantly less compared to the control, with the highest mortality (72%) in M. anisopliae treatment applied at early flowering (30 DAS). Relationship analysis showed that white grub density was significantly related to peanut yield. A regression of yield on number of damaged pods also supported that treatment at the early flowering caused the highest impact in terms of reducing damage to pods and improving yield. These results suggest that applying M. anisopliae at the early flowering stage optimizes survival of M. anisopliae in the soil profile, meaning greater probability of larvae contacting the pathogen, leading to greater mortality.
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References
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267
Bidochka MJ, Kamp AM, Lavender TM, Dekoning J, De Croos JNA (2001) Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: uncovering cryptic species? Appl Environ Microbiol 67:1335–1342. https://doi.org/10.1128/AEM.67.3.1335-1342.2001
Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512–530. https://doi.org/10.3852/07-202
Boetel MA, Majumdar A, Jaronski ST, Horsley RD (2012) Cover crop and conidia delivery system impacts on soil persistence of Metarhizium anisopliae (Hypocreales: Clavicipitaceae) in sugarbeet. Biocontrol Sci Tech 22:1284–1304. https://doi.org/10.1080/09583157.2012.725127
Bruck DJ (2005) Ecology of Metarhizium anisopliae in soilless potting media and the rhizosphere: implications for pest management. Biol Cont 32:155–163. https://doi.org/10.1016/j.biocontrol.2004.09.003
Bruck DJ (2009) Fungal entomopathogens in the rhizosphere. In: Roy HE, Vega FE, Chandler D, Goettel MS, Pell J, Wajnberg E (eds) The Ecology of Fungal Entomopathogens. Springer, Dordrecht, pp 103–112. https://doi.org/10.1007/978-90-481-3966-8_8
Chelvi CT, Thilagaraj WR, Nalini R (2011) Field efficacy of formulations of microbial insecticide Metarhizium anisopliae (Hyphocreales: Clavicipitaceae) for the control of sugarcane white grub Holotrichia serrata F (Coleoptera: Scarabidae). J Biopestic 4(2):186–189
Dar SA, Rather BA, Ajaz AK (2017) Insect pest management by entomopathogenic fungi. J Entomol Zool Stud 5(3):1185–1190
Douglas MR, Rohr JR, Tooker JF (2015) Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soya bean yield. J Appl Ecol 52:250–260. https://doi.org/10.1111/1365-2664.12372
Feng XJ, Liu CQ, Pu NN, Liu YT, Xu GC, Wang QL (2012) Application of Beauveria bassiana in controlling Holotrichia parallela. J Hebei Agri Sci 16(4):64–66
Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. Wiley, New York
Hallmann CA, Foppen RPB, van Turnhout CAM, de Kroon JE (2014) Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511:341–343. https://doi.org/10.1038/nature13531
Han XQ, Wu ZH, Zhang SQ, Zhang YX (2011) Investigation of dominant species of white grubs in peanut field and field control techniques in the eastern of Hebei province. J Hebei Agric Sci 15:27–29
Hu G, St. Leger RJ (2002) Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Appl Environ Microbiol 68(12):6383–6387. https://doi.org/10.1128/AEM.68.12.6383-6387.2002
Hu QB (2004) Research advance of occurrence and control of underground pest grub in China. Hubei Agric Sci 6:87–92
Imfeld G, Vuilleumier S (2012) Measuring the effects of pesticides on bacterial communities in soil: a critical review. Eur J Soil Biol 49:22–30. https://doi.org/10.1016/j.ejsobi.2011.11.010
Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Cont 116:36–45. https://doi.org/10.1016/j.biocontrol.2017.01.018
Jackson TA, Klein MG (2006) Scarabs as pests: a continuing problem. Coleopt Bull 60(mo 5):102–119. https://doi.org/10.1649/0010-065X(2006)60[102:SAPACP]2.0.CO;2
Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. Biocontrol 55:159–185. https://doi.org/10.1007/s10526-009-9248-3
Jiang YP, Ju Q, Jiang XJ, Zhao ZQ, Li X, Lu JJ, Jiang YS, Ni WL, Chen ZD, Wang GT (2013) Survey of peanut yield loss caused by white grub and its effect factors analysis. J Peanut Sci 42:42–46
Jin S, Zhou F (2018) Zero growth of chemical fertilizer and pesticide use: China's objectives, progress and challenges. J Resour Ecol 9:50–59. https://doi.org/10.5814/j.issn.1674-764x.2018.01.006
Johnson SN, Rasmann S (2015) Root-feeding insects and their interactions with organisms in the rhizosphere. Annu Rev Entomol 60:517–535. https://doi.org/10.1146/annurev-ento-010814-020608
Kessler P, Enkerli J, Schweizer C, Keller S (2004) Survival of Beauveria brongniartii in the soil after application as a biocontrol agent against the European cockchafer Melolontha melolontha. Biocontrol 49:563–581. https://doi.org/10.1023/B:BICO.0000036441.40227.ed
Liu X, Nong X, Liu C, Xi G, Zhang X, Zhang Z (2011) Biocontrol of peanut white grubs, Holotrichia parallela, using entomopathogenic fungus Metarhizium anisopliae at sowing period of peanut. Chin J Biol Cont 27:485–489
Liu X, Nong X, Su Y, Li X, Zhang Z (2014) An efficiently selective medium with dodine for quantitative isolation of Metarhizium anisolpliae in soil. Chin J Biol Control 30:552–557
Liu X, Nong X, Wang Q, Li X, Wang G, Cao G, Zhang Z (2016) Persistence and proliferation of a Chinese Metarhizium anisopliae ss isolate in the peanut plant root zone. Biocontrol Sci Tech 26(6):746–758. https://doi.org/10.1080/09583157.2016.1155106
Luo Z, Li K, Cao Y, Yin J, Zhang J, Zhang J, Shang G (2009) Investigations on soil-inhabiting pests in peanut fields in Henan. Plant Prot 35:104–108
Martínez-García LB, Korthals G, Brussaard L, Jørgensen HB, De Deyn GB (2018) Organic management and cover crop species steer soil microbial community structure and functionality along with soil organic matter properties. Agr Ecosyst Environ 263:7–17. https://doi.org/10.1016/j.agee.2018.04.018
Maute K, French K, Story P, Bull CM, Hose GC (2017) Short and long-term impacts of ultra-low-volume pesticide and biopesticide applications for locust control on non-target arid zone arthropods. Agr Ecosyst Environ 240:233–243. https://doi.org/10.1016/j.agee.2017.02.024
Milner RJ, Samson P, Morton R (2003) Persistence of conidia of Metarhizium anisopliae in sugarcane fields: effect of isolate and formulation on persistence over 3.5 years. Biocontrol Sci Technol 13(5):507–516. https://doi.org/10.1080/0958315031000140965
Nong X, Liu C, Lu X, Wang Q, Wang G, Zhang Z (2011) Laboratory evaluation of entomopathogenic fungi against the white grubs, Holotrichia oblita and Anomala corpulenta (Coleoptera: Scarabaeidae) from the field of peanut, Arachis hypogaea. Biocontrol Sci Technol 21(5):593–603. https://doi.org/10.1080/09583157.2011.566324
Nong X, Tu X, Zhang Z, Li C (2007) Factors affecting solid fermentation of Metarhizium anisopliae R8–4. Chin J Biol Control 23:228–232
Paulitz TC (2000) Population dynamics of biocontrol agents and pathogens in soils and rhizospheres. Eur J Plant Pathol 106:401–413. https://doi.org/10.1023/A:1008733927515
Pava-Ripoll M, Angelini C, Weiguo Fang W, Wang S, Posada FJ, St. Leger R (2011) The rhizosphere-competent entomopathogen Metarhizium anisopliae expresses a specific subset of genes in plant root exudate. Microbiology 157:47–55. https://doi.org/10.1099/mic.0.042200-0
Pilz C, Enkerli J, Wegensteiner R, Keller S (2011) Establishment and persistence of the entomopathogenic fungus Metarhizium anisopliae in maize fields. J Appl Entomol 135:393–403. https://doi.org/10.1111/j.1439-0418.2010.01566.x
Pu ZL, Li ZZ (1996) Insect mycology. Anhui Science and Technology Press, Hefei, pp 362–454
Quesada-Moraga E, Navas-Cortés JA, Maranhao EAA, Ortiz-Urquiza A, Santiago-Álvarez C (2007) Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycol Res 111:947–966. https://doi.org/10.1016/j.mycres.2007.06.006
Sattler C, Kächele H, Verch G (2007) Assessing the intensity of pesticide use in agriculture. Agr Ecosyst Environ 119:299–304. https://doi.org/10.1016/j.agee.2006.07.017
Schäfer RB, Liess M, Altenburger R, Filser J, Hollert H, Roß-Nickoll M, Schäffer A, Scheringe M (2019) Future pesticide risk assessment: narrowing the gap between intention and reality. Environ Sci Eur 31:21. https://doi.org/10.1186/s12302-019-0203-3
Shao H, Zhang Y (2017) Non-target effects on soil microbial parameters of the synthetic pesticide carbendazim with the biopesticides cantharidin and norcantharidin. Sci Rep 7(5521):1–12. https://doi.org/10.1038/s41598-017-05923-8
Skinner M, Parker BL, Kim JS (2014) Role of entomopathogenic fungi in integrated pest management. In: Integrated Pest Management. Academic Press, Cambridge, pp 169–191. https://doi.org/10.1016/B978-0-12-398529-3.00011-7
St. Leger RJ (2008) Studies on adaptations of Metarhizium anisopliae to life in the soil. J Invertebr Pathol 98:271–276. https://doi.org/10.1016/j.jip.2008.01.007
Tiago PV, Carneiro-Leao MP, Malosso E, De Oliveira NT, Lima EADLA (2012) Persistence and effect of Metarhizium anisopliae in the fungal community of sugarcane soil. Biocontrol 57:653–661. https://doi.org/10.1007/s10526-012-9445-3
Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzón A, Ownley BH, Pell JK, Rangel DEN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159. https://doi.org/10.1016/j.funeco.2009.05.001
Villani MG, Krueger SR, Schroeder PC, Consolie F, Consolie NH, Preston-Wilsey LM, Roberts DW (1994) Soil application effects of Metarhizium anisopliae on Japanese beetle (Coleoptera: Scarabaeidae) behavior and survival in turfgrass microcosms. Environ Entomol 23:502–513. https://doi.org/10.1093/ee/23.2.502
Wang C, St. Leger RJ (2007) The MAD1 adhesin of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. Eukaryot Cell 6(5):808–816. https://doi.org/10.1128/EC.00409-06
Wang D, Fahad S, Saud S, Kamran M, Khan A, Khan MN, Hammad HM, Nasim W (2019) Morphological acclimation to agronomic manipulation in leaf dispersion and orientation to promote “Ideotype” breeding: evidence from 3D visual modeling of “super” rice (Oryza sativa L.). Plant Physiol Biochem 135:499–510. https://doi.org/10.1016/j.plaphy.2018.11.010
Wood TJ, Goulson D (2017) The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ Sci Pollut Res 24:17285–17325. https://doi.org/10.1007/s11356-017-9240-x
Xu Z (1991) White grub, an important insect pest of peanut and their control in China. In: Proceedings of a workshop on integrated pest management and insecticide resistance management (IPM/IRM) in legume crops in Asia, Chiang Mai, March 1991. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, Andhra Pradesh 502324, India. p 15.
Yang H, Qin CS, Chen YM, Zhang GY, Dong LH, Wan SQ (2019) Persistence of Metarhizium (Hypocreales: Clavicipitaceae) and Beauveria bassiana (Hypocreales: Clavicipitaceae) in tobacco soils and potential as biocontrol agents of Spodoptera litura (Lepidoptera: Noctuidae). Environ Entomol 48:147–155. https://doi.org/10.1093/ee/nvy161
Acknowledgements
We would like to thank Chunqin Liu and her team members of Cangzhou Agricultural and Forest Science Academy, Hebei, China for participating in the soil treatment and planting management. Thanks to Chikako van Koten (AgResearch Ltd.) for assistance in analysis of white grub and peanut data. We would also like to thank LetPub for providing linguistic assistance during the preparation of this manuscript.
Funding
This study was financially supported by National Key R&D Program of China under project Nos. 2018YFD0201000 and 2017YFD0201205, and the Earmarked Fund for China Agriculture Research System (CARS-34-07B).
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Conceptualization, XL, XN and ZZ; Formal analysis, QW; Investigation, XL, XL and XN; Methodology, ZZ; Resources, GW, HU, QW and HVH; Supervision, XN; Validation, HVH; Visualization, HVH; Writing—original draft, XL, XN and ZZ; Writing—review and editing, XN, MRM and HU.
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Li, X., Liu, X., Nong, X. et al. Peanut early flowering stage is beneficial to Metarhizium anisopliae survival and control of white grub larvae. 3 Biotech 10, 188 (2020). https://doi.org/10.1007/s13205-020-02178-5
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DOI: https://doi.org/10.1007/s13205-020-02178-5