Abstract
Global demand for environmentally friendly grapevine cultivation and pest control has necessitated an improved understanding of the relationship between soil properties and beneficial, naturally occurring antagonists such as entomopathogenic fungi (EPF). Sixty six soil samples were collected from 22 vineyards in the Western Cape, South Africa. The association between soil nutrient status and EPF prevalence was examined. Fungi were isolated with methods of insect baiting and selective media. In addition, fungal isolates were tested against a key grapevine pest, Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). Pathogenicity of fungal strains against P. ficus was assessed with an immersion bioassay at a concentration of 1 × 108 conidia ml–1. Twenty-three fungal strains were isolated and correspondence analysis of data indicated a positive association between EPF (Metarhizium robertsii (Hypocreales: Clavicipitaceae) and Clonostachys rosea f. catenulata [Hypocreales: Bionectriaceae]) occurrence and optimum to high levels of soil-based macronutrients (C, N and Ca). Logistic regression revealed that K was positively correlated with M. robertsii (estimate = 0.03 ± 0.01; P < 0.05; odds ratio = 1.03). Strains of Beauvaria bassiana (Hypocreales: Cordycipitaceae) caused the highest mortalities (77.0 ± 2.0% to 87.0 ± 3.0%). This study showed that some soil nutrient properties corresponded to greater occurrence of EPF in grapevine soils.
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References
Abaajeh AR, Nchu F (2015) Isolation and pathogenicity of some South African entomopathogenic fungi (Ascomycota) against eggs and larvae of Cydia pomonella (Lepidoptera: Tortricidae). Biocontrol Sci Technol 25:828–842
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267
Amutha M, Banu JG (2017) Variation in mycosis of entomopathogenic fungi on mealybug, Paracoccus marginatus (Homoptera: Pseudococcidae). Proc Natl Acad Sci India B 87(2):343–349
Anwar W, Ali S, Nawaz K, Iftikhar S, Javed MA, Hashem A, Alqarawi AA, Abd_Allah EF, Akhter A (2018) Entomopathogenic fungus Clonostachys rosea as a biocontrol agent against whitefly (Bemisia tabaci). Biocontrol Sci Technol 28(8):750–760
Bargmann CJ (2003) Geology and Wine 7. Geology and wine production in the Coastal Region, Western Cape Province. South Africa. Geoscience Can 30(4):161–182
Bargmann CJ (2005) Geology and wine in South Africa. Geoscientist 15:4–8
Bemlab (2016) Soil analysis norms. Available via DIALOG. http://www.bemlab.co.za/uploads/GENERIC%20SOIL%20ANALYSIS%20NORMS_a.pdf. Accessed 19 July 2016
Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512–530
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
Bruck DJ (2010) Fungal endophyte in the rhizophere. BioControl 55:103–112
Campbell CR, Plank CO (1998) Preparation of plant tissue for laboratory analysis. In: Kalra YP (ed) Handbook of reference methods for plant analysis. CRC Press, Boca Raton, pp 37–49
Chandler D, Hay D, Reid AP (1997) Sampling and occurrence of entomopathogenic fungi and nematodes in UK soils. Appl Soil Ecol 5(2):133–141
Cooke WB (1968) Carbon/nitrogen relationships of fungus culture media. Mycopathologia 34(3):305–316
Crous CJ, Burgess TI, Le Roux JJ, Richardson DM, Slippers B, Wingfield MJ (2017) Ecological disequilibrium drives insect pest and pathogen accumulation in non-native trees. AoB Plants 9:plw081
Daane KM, Almeida RPP, Bell VA, Walker JTS, Botton M, Fallahzadeh M, Mani M, Miano JL, Sforza R, Walton VM, Zaviezo T (2012) Biology and management of mealybugs in vineyards. In: Bostanian NJ, Vincent C, Isaacs R (eds) Arthropod management in vineyards: pests, approaches, and future directions. Springer, New York, pp 271–307
du Plessis JA, Schloms B (2017) An investigation into the evidence of seasonal rainfall pattern shifts in the Western Cape, South Africa. J S Afr Inst Civ Eng 59(4):47–55
Epstein L, Bassein S (2003) Patterns of pesticide use in California and the implications for strategies for reduction of pesticides. Annu Rev Phytopathol 41:351–375
Feng MG, Poprawski TJ, Khachatourians GG (1994) Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control—current status. Biocontrol Sci Technol 4:3–34
Fernandez-Cornejo J (1998) Environmental and economic consequences of technology adoption: IPM in viticulture. Agric Econ 18:145–155
Frac M, Hannula SE, Bełka M, Jędryczka M (2018) Fungal biodiversity and their role in soil health. Front Microbiol 9:707
Gaskin RE, Manktelow DW, Elliott GS (2002) New adjuvant technology for pesticide use on wine grapes. NZ Plant Prot 55:154–158
Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330
Goble TA (2009) Investigation of entomopathogenic fungi for control of false codling moth, Thaumatotibia leucotreta, Mediterranean fruit fly, Ceratitis capitata and Natal fruit fly, C. rosea in South African Citrus. Master’s thesis, Rhodes University, Grahamstown
Goettel MS (1984) A simple method for mass culturing entomopathogenic hyphomycete fungi. J Microbiol Methods 3:15–20
Gouli V, Gouli S, Marcelino JAP, Margaret S, Parker BL (2013) Entomopathogenic fungi associated with exotic invasive insect pests in Northeastern forests of the USA. Insects 4:631–645
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9. Available via DIALOG. https://folk.uio.no/ohammer/past/. Accessed 16 Dec 2018
Hatting J, Hazir S, Macucwa G, Jooste H, Jankielsohn A (2004) Isolation of entomopathogens from South African soils using the Galleria mellonella-bait technique. In: Proceedings of the 37th annual meeting of the Society for Invertebrate Pathology
Ho WC, Ko WH (1997) A simple method for obtaining single-spore isolates of fungi. Bot Bull Acad Sin 38:41–44
Huber A, Bach M, Frede HG (2000) Pollution of surface waters with pesticides in Germany: modeling non-point source inputs. Agric Ecosyst Environ 80:191–204
Jabbour R, Barbercheck ME (2009) Soil management effects on entomopathogenic fungi during the transition to organic agriculture in a feed grain rotation. Biol Control 51:435–443
Jones GV, Davis RE (2000) Climatic influences on grapevine phenology, grape composition, and wine production and quality for Bordeaux, France. Am J Enol Vitic 51:249–261
Kepler RM, Humber RA, Bischoff JF, Rehner SA (2014) Clarification of generic and species boundaries for Metarhizium and related fungi through multigene phylogenetics. Mycologia 106:811–829
Klingen I, Eilenberg J, Meadow R (2002) Effects of farming system, field margins and bait insect on the occurrence of insect pathogenic fungi in soils. Agric Ecosyst Environ 91:191–198
Koorem K, Gazol A, Öpik M, Moora M, Saks Ü, Uibopuu A, Sõber V, Zöbel M (2014) Soil nutrient content influences the abundance of soil microbes but not plant biomass at the small-scale. PLoS ONE 9(3):e91998
Lazcano C, Gómez-Brandón M, Revilla P, Domínguez J (2012) Short-term effects of organic and inorganic fertilizers on soil microbial community structure and function: a field study with sweet corn. Biol Fertil Soils 49:723–733
Medo J, Cagáň L (2011) Factors affecting the occurrence of entomopathogenic fungi in soils of Slovakia as revealed using two methods. Biol Control 15(2):200–208
Mishra S, Malik A (2012) Nutritional optimization of a native Beauveria bassiana isolate (HQ917687) pathogenic to housefly Musca domestica L. J Parasit Dis 37(2):199–207
Mohamed GS (2016) Virulence of entomopathogenic fungi against the vine mealy bug, Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). Egypt J Biol Pest Control 26:47–51
Nelson PE, Toussom TA, Marasas WFO (1983) Fusarium species: an illustrated manual for identification. Pennsylvania State University Press, University Park
Non-Affiliated Soil Analysis Work Committee (1990) Handbook of standard soil testing methods for advisory purposes. Soil Science Society of South Africa, Pretoria
Ownley BH, Pereira RM, Klingeman WE (2004) Beauveria bassiana, a dual purpose biocontrol organism, with activity against insect pests and plant pathogens. In: Lartey RT, Caesar A (eds) Emerging concepts in plant health management. Research Signpost, Thiruvananthapuram, pp 255–269
Pell JK, Hannam JJ, Steinkraus DC (2010) Conservation biological control of entomopathogens. BioControl 55:187–198
Pu XY, Feng MG, Shi CH (2005) Impact of three application methods on the field efficacy of a Beauveria bassiana-based myco-insecticide against the false-eye leafhopper, Empoasca vitis (Homoptera: Cicadellidae) in the tea canopy. Crop Prot 24:167–175
Quesada-Moraga E, Navas-Cortés JA, Maranhao EAA (2007) Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycol Res 111:947–966
Raya-Dáaz S, Sánchez-Rodríguez AR, Segura-Fernández JM, del Campillo MdC, Quesada-Moraga E (2017) Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates. PLoS ONE 12(10):e0185903
Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97(1):84–98
Safavi SA, Shah FA, Pakdel AK (2007) Effect of nutrition on growth and virulence of the entomopathogenic fungus Beauveria bassiana. FEMS Microbiol Lett 270:116–123
Sharma L, Gonçalves F, Oliveira I, Torres L, Marques G (2018a) Insect-associated fungi from naturally mycosed vine mealybug Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). Biocontrol Sci Technol 28(2):122–141
Sharma L, Oliveira I, Torres L, Marques G (2018b) Entomopathogenic fungi in Portuguese vineyards soils: suggesting a “Galleria-Tenebrio-bait method” as bait-insects Galleria and Tenebrio significantly underestimate the respective recoveries of Metarhizium (robertsii) and Beauveria (bassiana). MycoKeys 38:1–23
Stenekamp D (2011) Optimization of a mass-rearing system to produce codling moth, Cydia pomonella, for a Sterile Insect Release programme in South Africa. Dissertation presented for the Degree of Doctor of Philosophy, Faculty of AgriSciences, Stellenbosch University
Strasser H, Vey A, Butt TM (2000) Are there any risks in using entomopathogenic fungi for pest control, with particular reference to the bioactive metabolites of Metarhizium, Tolypocladium and Beauveria species? Biocontrol Sci Technol 10:717–735
Sutton JC, Liu W, Huang R, Owen-Going N (2002) Ability of Clonostachys rosea to establish and suppress sporulation potential of Botrytis cinerea in de-leafed stems of hydroponic greenhouse tomatoes. Biocontrol Sci Technol 12:413–425
Tkaczuk C, Król A, Majchrowska-Safaryan A, Nicewicz Ł (2014) The occurrence of entomopathogenic fungi in soils from fields cultivated in a conventional and organic system. J Ecol Eng 15:137–144
Tsvuura Z, Avolio ML, Kirkman KP (2017) Nutrient addition increases biomass of soil fungi: evidence from a South African grassland. S Afr J Plant Soil 34:71–73
Tuininga AR, Miller JL, Morath SU, Daniels TJ, Falco RC, Marchese M, Sahabi S, Rosa D, Stafford KC III (2009) Isolation of entomopathogenic fungi from soils and Ixodes scapularis (Acari: Ixodidae) ticks: prevalence and methods. J Med Entomol 46(3):557–565
Uzman D, Pliester J, Leyer I, Entling MH, Reineke A (2019) Drivers of entomopathogenic fungi presence in organic and conventional vineyard soils. Appl Soil Ecol 133:89–97
Walton VM, Pringle KL (2004) Vine mealybug, Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae), a key pest in South African vineyards. A review. S Afr J Enol Vitic 25:54–62
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols. A guide to methods and applications. Academic, San Diego, pp 315–322
Zhang L, Yang J, Niu Q (2008) Investigation on the infection mechanism of the fungus Clonostachys rosea against nematodes using the green fluorescent protein. Appl Microbiol Biotechnol 78:983–990
Zhu Y, Pan J, Qiu J, Guan X (2008) Optimization of nutritional requirements for mycelial growth and sporulation of entomogenous fungus Aschersonia aleyrodis Webber. Braz J Microbiol 39(4):770–775
Acknowledgements
The authors of this paper would like to convey their thanks and appreciation to the National Research Foundation, South Africa and Cape Peninsula University of Technology (University Research Fund; Grant No. R166) for funding this study. Prof, Karin Jacobs at the University of Stellenbosch contributed to fungal identification. We thank Dr. Marilize Le Roes-Hill (Biocatalysis and Technical Biology Research Group, CPUT) for comments that greatly improved the manuscript. The authors thank Entomon Technologies (Pty.) Ltd. in Stellenbosch for supplying the different life stages of codling moths.
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Supplementary file1 (PDF 3823 kb) Supplementary Fig. S1 Neighbour-joining trees based on ITS and BTub sequences showing relationships to taxonomically similar reference strains in the following genera: Metarhizium and Beauveria (1), Clonostachys (2), Fusarium (3) and Talaromyces and Aspergillus (4). The corresponding bootstrap values are indicated at each branch node
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Supplementary file2 (DOC 44 kb) Supplementary Table 1 Sequence identification of extracted DNA from entomopathogenic fungal isolates collected from vineyards in the Cape Winelands, South Africa
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Moloinyane, S., Addison, P., Achiano, K.A. et al. Association between chemical properties of vineyard soils and occurrence of entomopathogenic fungi causing different levels of mortality in Planococcus ficus. BioControl 65, 197–209 (2020). https://doi.org/10.1007/s10526-019-09989-3
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DOI: https://doi.org/10.1007/s10526-019-09989-3