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Wireworm damage reduction in potatoes with an attract-and-kill strategy using Metarhizium brunneum

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Abstract

Innovative wireworm control strategies are required to implement integrated pest management on the basis of the (EC) No regulation 1107/2009 and Directive 2009/128/EC. Entomopathogenic fungi, such as Metarhizium brunneum (Metschnikoff) Sorokin, are potential biological control agents for wireworm control but do not achieve high control efficacies in the field when applied as a conidia suspension. In a 2-year study, wireworm control with a novel attract-and-kill strategy aimed at enhancing M. brunneum efficacies in organic potato production systems in Lower Saxony, Germany. The approach is based on the attraction of wireworms (Agriotes spp. Eschscholtz) towards an artificial carbon dioxide-emitting source, using baker’s yeast (Saccharomyces cerevisiae Meyen ex Hansen) in combination with M. brunneum conidia for wireworm infection. Both components were encapsulated in alginate as a carrier material and applied in a mixture with two types of beads (one for encapsulated yeast and one for M.brunneum conidia). An application of these beads within the potato rows during potato planting reduced wireworm tuber damage by 37–75% relative to the untreated control and was able to enhance the efficacy of M. brunneum by up to 35% through an attract-and-kill approach compared to beads without a carbon dioxide source only. This strategy offers a high potential to promote biological wireworm control as an alternative to insecticide use by potentially reducing the inoculum compared to an inundate M. brunneum conidia release strategy.

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References

  • Abbott WS (1987) Abbotts formula—a method of computing the effectiveness of an insecticide. J Am Mosquito Contr 3:302–303

    CAS  Google Scholar 

  • Anonymous (2005) Wireworms. Bull OEPP/EPPO Bull 35:179–182

    Article  Google Scholar 

  • Anonymous (2012) Design and analysis of efficacy evaluation trials. Bull OEPP/EPPO Bull 42:367–381

    Article  Google Scholar 

  • Bidochka MJ, Kasperski JE, Wild GAM (1998) Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Can J Bot 76:1198–1204

    Google Scholar 

  • Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512–530. doi:10.3852/07-202

    Article  CAS  PubMed  Google Scholar 

  • Cherry R, Stansly P (2008) Abundance and spatial distribution of wireworms (Coleoptera: Elateridae) in Florida sugarcane fields on muck versus sandy soils. Fla Entomol 91:383–387

    Article  Google Scholar 

  • Crawley MJ (2013) The R book, 2nd edn. Wiley, London

    Google Scholar 

  • Doane JF, Lee YW, Klingler J, Westcott ND (1975) Orientation response of Ctenicera destructor and other wireworms (Coleoptera: Elateridae) to germinating grain and to carbon-dioxide. Can Entomol 107:1233–1252

    Article  Google Scholar 

  • Eckard S, Ansari MA, Bacher S, Butt TM, Enkerli J, Grabenweger G (2014) Virulence of in vivo and in vitro produced conidia of Metarhizium brunneum strains for control of wireworms. Crop Prot 64:137–142. doi:10.1016/j.cropro.2014.06.017

    Article  Google Scholar 

  • European Food Safety Authority (2013) Conclusion on the peer review of the pesticide risk assessment for bees for the active substance fipronil. EFSA J 11(5):1–51. doi:10.2903/j.efsa.2013.3158

    Google Scholar 

  • European Parliament and the Council of the European Union (2009a) Directive 2009/128/EC of the European Parliament and of the Council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides. Off J Eur Union 52:71–86. doi:10.3000/17252555.L_2009.309.eng

    Google Scholar 

  • European Parliament and the Council of the European Union (2009b) Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC. Off J Eur Union 52:1–50. doi:10.3000/17252555.L_2009.309.eng

    Google Scholar 

  • Fox CJS (1961) The distribution and abundance of wireworms in the Annapolis Valley of Nova Scotia. Can Entomol 93:276–279

    Article  Google Scholar 

  • Furlan L (2004) The biology of Agriotes sordidus Illiger (Col., Elateridae). J Appl Entomol 128:696–706. doi:10.1111/j.1439-0418.2004.00914.x

    Article  Google Scholar 

  • Furlan L, Bonetto C, Finotto A, Lazzeri L, Malaguti L, Patalano G, Parker W (2010) The efficacy of biofumigant meals and plants to control wireworm populations. Ind Crop Prod 31:245–254. doi:10.1016/j.indcrop.2009.10.012

    Article  CAS  Google Scholar 

  • Gillespie AT, Claydon N (1989) The use of entomogenous fungi for pest-control and the role of toxins in pathogenesis. Pestic Sci. doi:10.1002/ps.2780270210

    Google Scholar 

  • Gunasekara AS, Truong T, Goh KS, Spurlock F, Tjeerdema RS (2007) Environmental fate and toxicology of fipronil. J Pestic Sci 32:189–199. doi:10.1584/jpestics.RO7-02

    Article  CAS  Google Scholar 

  • Hack H, Gall H, Klemke T, Klose R, Meier U, Stauss R, Witzen-Berger A (2001) Potato. In: Meier U (ed) Growth stages of mono-and dicotyledonous plants, vol 2., EditionFederal Biological Research Centre for Agriculture and Forestry, Germany, pp 44–51

    Google Scholar 

  • Hartigan JA, Kleiner B (1981) Mosaics for contingency tables. In: Eddy WF (ed) Computer Science and Statistics: proceedings of the 13th Symposium on the Interface. Springer-Verlag, New York, pp 268–273

    Chapter  Google Scholar 

  • Hartigan JA, Kleiner B (1984) A mosaic of television ratings. Am Stat 38:32–35. doi:10.2307/2683556

    Google Scholar 

  • Hermann A, Brunner N, Hann P, Wrbka T, Kromp B (2013) Correlations between wireworm damages in potato fields and landscape structure at different scales. J Pest Sci 86:41–51. doi:10.1007/s10340-012-0444-z

    Article  Google Scholar 

  • Hofmann H (2003) Constructing and reading mosaicplots. Comput Stat Data An 43:565–580

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363. doi:10.1002/bimj.200810425

    Article  Google Scholar 

  • Hu G, St Leger J (2002) Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Appl Environ Microb 68:6383–6387. doi:10.1128/Aem.68.12.6383-6387.2002

    Article  CAS  Google Scholar 

  • Humber RA (2012) Identification of entomopathogenic fungi. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, vol 2., Academic PressLondon, UK, pp 151–187

    Chapter  Google Scholar 

  • Hyslop JA (1915) Wireworms attacking cereal and forage crops. In: Bulletin of the US Department of Agriculture no. 156, U.S. Department of Agriculture, Washington, D.C., pp 1–34

  • Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents. progress, problems and potential. CABI Publishing, Wallingford, pp. 23–69

  • Inglis GD, Enkerli J, Goettel MS (2012) Laboratory techniques used for entomopathogenic fungi: hypocreales. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, 2nd edn. Academic Press, London, pp 189–253

    Chapter  Google Scholar 

  • Inyang EN, McCartney HA, Oyejola B, Ibrahim L, Pye BJ, Archer SA, Butt TM (2000) Effect of formulation, application and rain on the persistence of the entomogenous fungus Metarhizium anisopliae on oilseed rape. Mycol Res 104:653–661. doi:10.1017/S0953756200002641

    Article  Google Scholar 

  • Jansson RK, Seal DR (1994) Biology and management of wireworm on potato. In: Zehnder GW, Powelson ML, Jansson RK, Raman KV (eds) Proceedings of the international conference on “Advances in Potato Pest Biology and Management”. American Phytopathological Society Press, St. Paul, pp 31–53

    Google Scholar 

  • Jaronski ST (2007) Soil ecology of the entomopathogenic Ascomycetes: A critical examination of what we (think) we know. In: Ekesi S, Maniania NK (eds) Use of entomopathogenic fungi in biological pests management. Research Signpost, Trivandrum, India, pp. 91–143

  • Johnson SN, Anderson EA, Dawson G, Griffiths DW (2008) Varietal susceptibility of potatoes to wireworm herbivory. Agric For Entomol 10:167–174. doi:10.1111/j.1461-9563.2008.00372.x

    Article  Google Scholar 

  • Kabaluk JT, Vernon RS, Goettel MS (2007) Mortality and infection of wireworm, Agriotes obscurus [Coleoptera : Elateridae], with inundative field applications of Metarhizium anisopliae. Phytoprotection 88:51–56

    Article  Google Scholar 

  • Kabaluk JT, Lafontaine JP, Borden JH (2015) An attract and kill tactic for click beetles based on Metarhizium brunneum and a new formulation of sex pheromone. J Pest Sci 88:707–716. doi:10.1007/s10340-015-0661-3

    Article  Google Scholar 

  • Kaplan EL, Meier P (1958) Nonparametric-estimation from incomplete observations. J Am Stat Assoc 53:457–481. doi:10.2307/2281868

    Article  Google Scholar 

  • Keiser A, Haberli M, Stamp P (2012) Drycore appears to result from an interaction between Rhizoctonia solani and wireworm (Agriotes ssp.) evidence from a 3-year field survey. Potato Res 55:59–67. doi:10.1007/s11540-012-9207-8

    Article  Google Scholar 

  • Keller S, Kessler P, Schweizer C (2003) Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metharhizium anisopliae. Biocontrol 48:307–319. doi:10.1023/A:1023646207455

    Article  Google Scholar 

  • Kölliker U, Biasio L, Jossi W (2011) Potential control of swiss wireworms with entomopathogenic fungi. IOBC/wprs Bull 66:517–520

    Google Scholar 

  • Lacey LA, Solter LF (2012) Initial handling and diagnosis of diseased invertbrates. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, vol 2. Academic Press, London

    Google Scholar 

  • Lafrance J (1968) The seasonal movements of wireworms (Coleoptera: Elateridae) in relation to soil moisture and temperature in the organic soils of southwestern Quebec. Can Entomol 100:801–807

    Article  Google Scholar 

  • Lundegardh H (1927) Carbon dioxide evolution and crop growth. Soil Sci 23:417–453

    Article  CAS  Google Scholar 

  • Meyer D, Zeileis A, Hornik K (2006) The strucplot framework: visualizing multi-way contingency tables with vcd. J Stat Softw 17:1–48

    Article  Google Scholar 

  • Meyer D, Zeileis A, Hornik K (2014) vcd: Visualizing categorical data. R package version 1.3-2

  • Meyling NV, Eilenberg J (2007) Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol Control 43:145–155. doi:10.1016/j.biocontro1.2007.07.007

    Article  Google Scholar 

  • Mietkiewski RT, Pell JK, Clark SJ (1997) Influence of pesticide use on the natural occurrence of entomopathogenic fungi in arable soils in the UK: field and laboratory comparisons. Biocontrol Sci Technol 7:565–575

    Article  Google Scholar 

  • Neuhoff D, Christen C, Paffrath A, Schepl U (2007) Approaches to wireworm control in organic potato production. IOBC/wprs Bull 30:65–68

    Google Scholar 

  • Parker WE, Howard JJ (2001) The biology and management of wireworms (Agriotes spp.) on potato with particular reference to the U.K. Agric For Entomol 3:85–98. doi:10.1046/j.1461-9563.2001.00094.x

    Article  Google Scholar 

  • 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. doi:10.1111/j.1439-0418.2010.01566.x

    Article  Google Scholar 

  • Posadas JB, Comerio RM, Mini JI, Nussenbaum AL, Lecuona RE (2012) A novel dodine-free selective medium based on the use of cetyl trimethyl ammonium bromide (CTAB) to isolate Beauveria bassiana, Metarhizium anisopliae sensu lato and Paecilomyces lilacinus from soil. Mycologia 104:974–980. doi:10.3852/11-234

    Article  CAS  PubMed  Google Scholar 

  • Raich JW, Schlesinger WH (1992) The global carbon-dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus B 44:81–99. doi:10.1034/j.1600-0889.1992.t01-1-00001.x

    Article  Google Scholar 

  • Rixon AJ, Bridge BJ (1968) Respiratory quotient arising from microbial activity in relation to matric suction and air filled pore space of soil. Nature 218:961–962. doi:10.1038/218961a0

    Article  CAS  PubMed  Google Scholar 

  • Rovira AD (1953) Use of the warburg apparatus in soil metabolism studies. Nature 172:29–30. doi:10.1038/172029b0

    Article  CAS  PubMed  Google Scholar 

  • Saxton KE, Rawls WJ, Romberger JS, Papendick RI (1986) Estimating generalized soil-water characteristics from texture. Soil Sci Soc Am J 50:1031–1036

    Article  Google Scholar 

  • Scheepmaker JWA, Butt TM (2010) Natural and released inoculum levels of entomopathogenic fungal biocontrol agents in soil in relation to risk assessment and in accordance with EU regulations. Biocontrol Sci Technol 20(5):503–552

    Article  Google Scholar 

  • Schumann M, Patel A, Vidal S (2014a) Soil application of an encapsulated CO2 source and its potential for management of western corn rootworm larvae. J Econ Entomol 107:230–239. doi:10.1603/Ec13344

    Article  CAS  PubMed  Google Scholar 

  • Schumann M, Toepfer S, Vemmer M, Patel A, Kuhlmann U, Vidal S (2014b) Field evaluation of an attract and kill strategy against western corn rootworm larvae. J Pest Sci 87:259–271. doi:10.1007/s10340-013-0551-5

    Article  Google Scholar 

  • Shah FA, Wang CS, Butt TM (2005) Nutrition influences growth and virulence of the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol Lett 251:259–266. doi:10.1016/j.femsle.2005.08.010

    Article  CAS  PubMed  Google Scholar 

  • St. Leger RJ (2008) Studies on adaptations of Metarhizium anisopliae to life in the soil. J Invertebr Pathol 98:271–276. doi:10.1016/j.jip.2008.01.007

    Article  PubMed  Google Scholar 

  • Strasser H, Forer A, Schinner F (1996) Development of media for the selective isolation and maintenance of virulence of Beauveria brongniartii. In: Jackson TA, Glare TR (eds) Proceedings 3rd international workshop on microbial control of soil dwelling pests. AgResearch, Lincoln, New Zealand, pp. 125–130

  • R Development Core Team (2013) R: a language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria. http://www.R-project.org/

  • Thomas CA (1940) The biology and control ow wireworms: A review of the literature. The Pennsylvania State College, School of Agriculture and Experiment Station, State College, p 392

    Google Scholar 

  • Traugott M, Benefer CM, Blackshaw RP, van Herk WG, Vernon RS (2015) Biology, ecology, and control of elaterid beetles in agricultural land. Annu Rev Entomol 60:313–334. doi:10.1146/annurev-ento-010814-021035

    Article  CAS  PubMed  Google Scholar 

  • Turpin HW (1920) The carbon dioxide of the soil air. Cornell University Agr Exp Sta, Memoir 32:315–362

    Google Scholar 

  • van Herk WG, Vernon RS (2007) Soil bioassay for studying behavioral responses of wireworms (Coleoptera: Elateridae) to insecticide-treated wheat seed. Environ Entomol 36:1441–1449. doi:10.1603/0046-225x(2007)36[1441:sbfsbr]2.0.co;2

    Article  PubMed  Google Scholar 

  • van Herk WG, Vernon RS, Moffat C, Harding C (2008a) Response of the pacific coast wireworm, Limonius canus, and the dusky wireworm, Agriotes obscurus (Coleoptera: Elateridae), to insecticide-treated wheat seeds in a soil bioassay. Phytoprotection 89:7–19

    Article  Google Scholar 

  • van Herk WG, Vernon RS, Tolman JH, Saavedra HO (2008b) Mortality of a wireworm, Agriotes obscurus (Coleoptera: Elateridae), after topical application of various insecticides. J Econ Entomol 101:375–383. doi:10.1093/jee/101.2.375

    Article  PubMed  Google Scholar 

  • Vanninen I (1996) Distribution and occurrence of four entomopathogenic fungi in Finland: effect of geographical location, habitat type and soil type. Mycol Res 100:93–101

    Article  Google Scholar 

  • Vanninen I, Tyni-Juslin J, Hokkanen H (2000) Persistence of augmented Metarhizium anisopliae and Beauveria bassiana in Finnish agricultural soils. Biocontrol 45:201–222. doi:10.1023/A:1009998919531

    Article  Google Scholar 

  • Vemmer M, Patel AV (2013) Review of encapsulation methods suitable for microbial biological control agents. Biol Control 67:380–389. doi:10.1016/j.biocontrol.2013.09.003

    Article  CAS  Google Scholar 

  • Vemmer M, Schumann M, Beitzen-Heineke W, French BW, Vidal S, Patel A (2016) Development of a CO2 releasing co-formulation based on starch Saccharomyces cerevisiae and Beauveria bassiana attractive towards western corn rootworm larvae. Pest Manag Sci. doi:10.1002/ps.4245

    PubMed  Google Scholar 

  • Vernon RS, van Herk WG (2013) Wireworms as pests of potato. In: Giordanengo P, Vincent C, Alyokhin A (eds) Insect pests of potato. Academic Press, Oxford, pp 103–164

    Chapter  Google Scholar 

  • Vernon RS, Van Herk WG, Clodius M, Harding C (2013) Further studies on wireworm management in Canada: damage protection versus wireworm mortality in potatoes. J Econ Entomol 106:786–799. doi:10.1603/Ec12180

    Article  CAS  PubMed  Google Scholar 

  • Vernon RS, van Herk WG, Clodius M, Tolman J (2016) Companion planting attract-and-kill method for wireworm management in potatoes. J Pest Sci. doi:10.1007/s10340-015-0707-6

    Google Scholar 

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Acknowledgements

These studies were funded by means of the 7th Framework Programme of the European Union 282767 as a part of the project INBIOSOIL (http://inbiosoil.uni-goettingen.de). We would like to thank Bianca Tappe, Daniel Kretschmar and Marie Nörtemann for their technical assistance, numerous students, in particular Thies Fellenberg, for their contribution, and Dr. Christian Ahl (Georg-August-Universität Göttingen, Germany) for conducting the soil analysis. Furthermore, we would like to thank Wilfried Dreyer (Ökoring AG, Visselhövede, Germany) for his professional support, Agroscope (Reckenholz, Switzerland) for providing the strain ART2825 and all farmers for providing field sites. Finally, we would like to thank Todd Kabaluk (Agriculture and Agri-Food Canada) for commenting on a draft of the manuscript.

Funding

Work on these studies was funded by means of the 7th Framework Programme of the European Union 282767 as a part of the project INBIOSOIL (http://inbiosoil.uni-goettingen.de).

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Brandl, M.A., Schumann, M., Przyklenk, M. et al. Wireworm damage reduction in potatoes with an attract-and-kill strategy using Metarhizium brunneum . J Pest Sci 90, 479–493 (2017). https://doi.org/10.1007/s10340-016-0824-x

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