Journal of Pest Science

, Volume 93, Issue 1, pp 275–290 | Cite as

Impact of granular carriers to improve the efficacy of entomopathogenic fungi against wireworms in spring wheat

  • Anamika Sharma
  • Stefan Jaronski
  • Gadi V. P. ReddyEmail author
Original Paper


Wireworms are a major concern for wheat growers and several other crops around the globe. Environmentally friendly management strategies are needed because the present conventional chemical seed treatments can be ineffective and pose environmental risks. While biological control of wireworms in a general sense has not been practical, use of entomopathogenic fungi (EPF) is one environmentally friendly solution for this problem. In 2017, granular formulations of three EPFs, on polenta and millet spent substrate carriers, were applied in furrow at planting, at two rates, against a water control and imidacloprid seed treatment in spring wheat in Montana, USA. The selected EPFs were Beauveria bassiana GHA, Metarhizium robertsii DWR356, M. robertsii DWR2009, applied as granular formulations at 11 kg ha−1 or 22 kg ha−1. In 2017, at Valier, DWR356, DWR2009 on millet carrier at 22.4 kg ha−1 provided greater yield, but all the treatments at lower rate were still cost-effective. In 2018, B. bassiana GHA and M. robertsii DWR2009 were retested along with B. bassiana ERL836 and M. brunneum F52. Millet carrier alone, GHA and ERL836 on millet carrier obtained cost-effective results at irrigated and non-irrigated sites in 2018. However, these were less cost-effective than imidacloprid as a seed treatment. The overall cost–benefit ratio of using EPF granules was higher in both the years compared to control. Millet on which the fungi were grown worked better than the other carriers. Further evaluation of the effect of the carrier while applying EPFs in furrow as granules is required.


Beauveria bassiana Metarhizium robertsii DWR356 Metarhizium robertsii DWR2009 Millet carrier Biological control Bioinsecticides 



This project is supported by the Montana Wheat and Barley Committee. This material is based upon work supported by the National Institute of Food and Agriculture, US Department of Agriculture, Multistate Hatch project (The Working Group on Improving Microbial Control of Arthropod Pests) under award Accn# 1014624. We thank our team members, John H Miller, Ramadevi Gadi, Debra A. Miller and Ramandeep Kaur Sandhi for their help in establishing the experiments. The authors would like to thank Mark Grubb and John Majerus, Jonathan Stoltz, Kevin Johnson and Mike Leys for providing the field sites to conduct field trails. We also thank summer intern Gabby Drishinski, Mikayla Connelly and Carley Ries for their help during this study.


This study was funded by Montana Wheat and Barley Committee (MDA/MWBC-CY5418-462) and Multistate Hatch project (Accession #1014624).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. Adhikari A, Reddy GVP (2017) Evaluation of trap crops for the management of wireworms in spring wheat in Montana. Arthropod Plant Interact 11:755–766CrossRefGoogle Scholar
  2. Andrews N, Ambrosino MD, Fisher GC, Rondon SI (2008) Wireworm: biology and nonchemical management in potatoes in the Pacific Northwest. Accessed 20 Feb 2018
  3. Ansari MA, Evans M, Butt TM (2009) Identification of pathogenic strains of entomopathogenic nematodes and fungi for wireworm control. Crop Prot 28:269–272CrossRefGoogle Scholar
  4. Antwi FB, Shrestha G, Reddy GVP, Jaronski ST (2018) Entomopathogens in conjunction with imidacloprid could be used to manage wireworms (Coleoptera: Elateridae) on spring wheat. Can Entomol 150:124–139CrossRefGoogle Scholar
  5. Biocare (2018) ATTRACAP®, protection against wireworms. Bundesamt für Ernährungssicherheit, Federal Office for Food Security, Austria, 2018. Assessed 5 Jan 2019
  6. Brandl MA, Schumann M, Przyklenk M, Vidal S (2017) Wireworm damage reduction in potatoes with an attract-and-kill strategy using Metarhizium brunneum. J Pest Sci 90:479–493CrossRefGoogle Scholar
  7. Butt TM, Ansari MA (2011) Exploiting synergies to optimise the impact of entomopathogenic fungi. In: Insect pathogens and insect entomopathogenic nematodes. 13th European meeting on biological control in IPM systems: proceedings of IOBC/WPRS working group, 19–23 June 2011, Innsbruck, Austria, pp 11–17Google Scholar
  8. Comstock JH, Slingerland MV (1891) Wireworms. Bull 33. Cornell University Agricultural Experiment Station, Geneva, NY USA.
  9. Ensafi P, Crowder DW, Esser AD, Zhao Z, Marshall JM, Rashed A (2018) Soil type mediates the effectiveness of biological control against Limonius californicus (Coleoptera: Elateridae). J Econ Entomol 111:2053–2058PubMedGoogle Scholar
  10. Ericsson JD, Kabaluk JT, Goettel MS, Myers JH (2007) Spinosad interacts synergistically with the insect pathogen Metarhizium anisopliae against the exotic wireworms Agriotes lineatus and Agriotes obscurus (Coleoptera: Elateridae). J Econ Entomol 100:31–38CrossRefPubMedGoogle Scholar
  11. Esser AD, Milosavljević I, Crowder DW (2015) Effects of neonicotinoids and crop rotation for managing wireworms in wheat crops. J Econ Entomol 108:1786–1794CrossRefPubMedGoogle Scholar
  12. Ester A, Huiting HF (2007) Controlling wireworms (Agriotes spp.) in a potato crop with biologicals. In: Invertebrate pathogens in biological control: present and future. 10th European meeting, Proceedings, 23–29 June 2005, Bari, Italy, pp 189–196Google Scholar
  13. Etzler FE (2013) Identification of economic wireworms using traditional and molecular methods. M.S. thesis dissertation. Montana State University, Bozeman, MontanaGoogle Scholar
  14. Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256CrossRefGoogle Scholar
  15. Filipchuk OD, Yaroshenko VA, Ismailov VY, Vyatkina G (1995) Effectiveness of biological and chemical preparations against tobacco pests. Agrokhimiya 8:81–86Google Scholar
  16. Fry RC, Fergusson-Kolmes LA, Kolmes SA, Villani MG (1997) Radiographic study of the response of Japanese beetle larvae (Coleoptera: Scarabaeidae) to soil-incorporated mycelial particles of Metarhizium anisopliae (Deuteromycetes). J N Y Entomol Soc 105:113–120Google Scholar
  17. 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 86:41–51CrossRefGoogle Scholar
  18. Higginbotham RW, Froese PS, Carter AH (2014) Tolerance of wheat (Poales: Poaceae) seedlings to wireworm (Coleoptera: Elateridae). J Econ Entomol 107:833–837CrossRefPubMedGoogle Scholar
  19. Jackson TA, Alves SB, Pereira RM (2000) Success in biological control of soil-dwelling insects by pathogens and nematodes. In: Gurr G, Wratten S (eds) Biological control: measures of success. Springer, Dordrecht, pp 271–296CrossRefGoogle Scholar
  20. Jansson RK, Seal D (1994) Biology and management of wireworms on potato. In: Zehnder GW, Powelson ML, Jansson RK, Raman KV (eds) Advances in potato pest biology and management. American Phytopathological Society, Minnesota, pp 31–53Google Scholar
  21. Jaronski ST (2007) Soil ecology of the entomopathogenic ascomycetes: a critical examination of what we (think) we know. In: Maniana K, Ekesi S (eds) Use of entomopathogenic fungi in biological pest management. Research SignPosts, Trivandrum, pp 91–144Google Scholar
  22. Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. Biocontrol 55:159–185CrossRefGoogle Scholar
  23. Jaronski ST (2013) Mycosis inhibits cannibalism by Melanoplus sanguinipes, M. differentialis, Schistocerca americana, and Anabrus simplex. J Insect Sci 13:122CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jaronski ST, Jackson MA (2008) Efficacy of Metarhizium anisopliae microsclerotial granules. Biocontrol Sci Technol 18:849–863CrossRefGoogle Scholar
  25. Jaronski ST, Jackson MA (2012) Mass production of entomopathogenic Hypocreales. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, 2nd edn. Elsevier, New York, pp 255–284CrossRefGoogle Scholar
  26. Jedlička P, Frouz J (2007) Population dynamics of wireworms (Coleoptera, Elateridae) in arable land after abandonment. Biologia 62:103–111CrossRefGoogle Scholar
  27. Kabaluk JT, Ericsson JD (2007) Metarhizium anisopliae seed treatment increases yield of field corn when applied for wireworm control. Agron J 99:1377–1381CrossRefGoogle Scholar
  28. Kabaluk JT, Goettel M, Erlandson M, Ericsson J, Duke G, Vernon R (2005) Metarhizium anisopliae as a biological control for wireworms and a report of some other naturally-occurring parasites. IOBC/WPRS Bull 28:109–115Google Scholar
  29. Kabaluk JT, Vernon RS, Goettel MS (2007) Mortality and infection of wireworm, Agriotes obscurus Coleoptera: Elateridae, with inundative field applications of Metarhizium anisopliae. Phytoprotection 88:51–56CrossRefGoogle Scholar
  30. Kabaluk T, Janmaat A, Sheedy C, Goettel M, Noronha C (2013) Agriotes spp. L., wireworms and click beetles (Coleoptera: Elateridae). In: Mason PG, Gillespie DR (eds) Biological control programmes in Canada 2001–2012. CABI, Wallingford, pp 72–82CrossRefGoogle Scholar
  31. Keller S (1994) The fungus Zoophthora elateridiphaga as an important mortality factor of the click beetle Agriotes sputator. J Invertebr Pathol 63:90–91CrossRefGoogle Scholar
  32. Kim JS, Kassa A, Skinner M, Hata T, Parker BL (2011) Production of thermotolerant entomopathogenic fungal conidia on millet grain. J Ind Microbiol Biotechnol 38:697–704CrossRefPubMedGoogle Scholar
  33. Kleespies RG, Ritter C, Mitkovets PV, Fatu AC, Schuster C, Zimmermann G, Burghause F, Feiertag S, Leclerque A (2013) A survey of microbial antagonists of Agriotes wireworms from Germany and Italy. J Pest Sci 86:99–106. CrossRefGoogle Scholar
  34. Landl M, Glauninger J (2011) Preliminary investigations into the use of trap crops to control Agriotes spp. (Coleoptera: Elateridae) in potato crops. J Pest Sci 86:85–90CrossRefGoogle Scholar
  35. Leclerque A, Mitkovets PV, Fatu AC, Schuster C, Kleespies RG (2013) Ribosomal RNA phylogeny of bacterial and fungal pathogens of Agriotes wireworms. J Pest Sci 86:107–113CrossRefGoogle Scholar
  36. Mascarin GM, Jaronski ST (2017) The production and uses of Beauveria bassiana as a microbial insecticide. World J Microbiol Biotechnol 32(11):177. Epub 2016 Sep 15 CrossRefGoogle Scholar
  37. Mburu DM, Ndung’u MW, Maniania NK, Hassanali A (2011) Comparison of volatile blends and gene sequences of two isolates of Metarhizium anisopliae of different virulence and repellency toward the termite Macrotermes michaelseni. J Exp Biol 214:956–962CrossRefPubMedGoogle Scholar
  38. Meyling NV, Pell JK (2006) Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecol Entomol 31:162–171CrossRefGoogle Scholar
  39. Mietkiewski R, Balazy S (2003) Persistent appearance of Cordyceps gracilis on Selatosomus-larvae near Siedlce (Poland). IOBC-WPRS Bull 26:39–42Google Scholar
  40. Milosavljević I, Esser AD, Crowder DW (2016) Effects of environmental and organic factors on soil-dwelling pest communities in cereal crops. Agric Ecosyst Environ 225:192–198CrossRefGoogle Scholar
  41. Mishra S, Kumar P, Malik A (2015) Effect of temperature and humidity on pathogenicity of native Beauveria bassiana isolate against Musca domestica L. J Parasit Dis 39:697–704CrossRefPubMedGoogle Scholar
  42. Morales-Rodriguez A, O’Neill RP, Wanner KW (2014) A survey of wireworm (Coleoptera: Elateridae) species infesting cereal crops in Montana. Pan-Pac Entomol 90:116–125CrossRefGoogle Scholar
  43. NRCS (1999) Soil survey staff, natural resources conservation service, United States department of agriculture. Web soil survey. Accessed 8 Feb 2018
  44. Ormond E (2007) The overwintering interactions of the seven spot ladybird (Coccinella septempunctata) and the entomopathogenic fungus Beauveria bassiana. Ph.D. thesis, Anglia Ruskin University, CambridgeGoogle Scholar
  45. 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 3:85–98CrossRefGoogle Scholar
  46. Rashed A, Rogers CW, Rashidi M, Marshall JM (2017) Sugar beet wireworm Limonius californicus damage to wheat and barley: evaluations of plant damage with respect to soil media, seeding depth, and diatomaceous earth. Arthropod Plant Interact 11:147–154CrossRefGoogle Scholar
  47. Reddy GVP, Tangtrakulwanich K, Wu S, Miller JH, Ophus VL, Prewett J, Jaronski ST (2014) Evaluation of the effectiveness of the entomopathogens for the management of wireworms (Coleoptera: Elateridae) on spring wheat. J Invertebr Pathol 120:43–49CrossRefPubMedGoogle Scholar
  48. Ritter C, Richter E (2013) Control methods and monitoring of Agriotes wireworms (Coleoptera: Elateridae). J Plant Dis Prot 120:4–15CrossRefGoogle Scholar
  49. SAS Institute Inc. (2018) In-database products, user’s guide, 5th edn. SAS Publishers, CaryGoogle Scholar
  50. Sharma A, Sandhi RK, Briar SS, Miller JH, Reddy GVP (2018) Assessing the performance of pea and lentil at different seeding densities as trap crops for the management of wireworms in spring wheat. J Appl Entomol. CrossRefGoogle Scholar
  51. Staudacher K, Schallhart N, Thalinger B, Wallinger C, Juen A, Traugott M (2013) Plant diversity affects behavior of generalist root herbivores, reduces crop damage, and enhances crop yield. Ecol Appl 23:1135–1145CrossRefPubMedGoogle Scholar
  52. Thomas CA (1932) The diseases of Elateridae (Coleoptera). Entomol News 43:149–155Google Scholar
  53. 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 60:313–334CrossRefPubMedGoogle Scholar
  54. van Herk WG, Vernon R (2013) Wireworm damage to wheat seedlings: effect of temperature and wireworm state. J Pest Sci 86:63–75CrossRefGoogle Scholar
  55. van Herk WG, Labun TJ, Vernon RS (2018) Efficacy of diamide, neonicotinoid, pyrethroid, and phenyl pyrazole insecticide seed treatments for controlling the sugar beet wireworm, Limonius californicus (Coleoptera: Elateridae), in spring wheat. J Entomol Soc Brit Columbia 115:86–100Google Scholar
  56. Vemmer M, Schumann M, Beitzen-Heineke W, French BW, Vidal S, Patel AV (2016) Development of a CO2-releasing coformulation based on starch, Saccharomyces cerevisiae and Beauveria bassiana attractive towards western corn rootworm larvae. Pest Manag Sci 72:2136–2145CrossRefPubMedGoogle Scholar
  57. Vernon RS (2010) Wireworm field guide: a guide to the identification and control of wireworms. Syngenta Crop Protection Canada Inc. Accessed 28 March 2018
  58. Vernon RS, van Herk WG (2012) Wireworms as pests of potato. In: Giordanengo P, Vincent C, Alyokhin A (eds) Insect pests of potato: global perspectives on biology and management. Academic Press, Amsterdam, pp 103–164Google Scholar
  59. Vernon RS, van Herk WG, Clodius M, Harding C (2009) Wireworm management I. Stand protection versus wireworm mortality with wheat seed treatments. J Econ Entomol 102:2126–2136CrossRefPubMedGoogle Scholar
  60. Vernon RS, van Herk WG, Clodius M, Harding C (2013) Crop protection and mortality of Agriotes obscurus wireworms with blended insecticidal wheat seed treatments. J Pest Sci 86:137–150CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Research Centers, Western Triangle Agricultural Research CenterMontana State University-BozemanConradUSA
  3. 3.USDA-ARS-Southern Insect Management Research UnitStonevilleUSA

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