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Journal of Pest Science

, Volume 87, Issue 2, pp 259–271 | Cite as

Field evaluation of an attract and kill strategy against western corn rootworm larvae

  • M. SchumannEmail author
  • S. Toepfer
  • M. Vemmer
  • A. Patel
  • U. Kuhlmann
  • S. Vidal
Original Paper

Abstract

The larvae of the invasive maize pest Diabrotica virgifera virgifera (Coleoptera; Chrysomelidae, western corn rootworm) hatch in the soil in spring and search for maize roots following CO2 gradients. CO2 is one cue that might be used as an attractant towards soil insecticides, a mechanism already shown in laboratory experiments. This study compared the efficacy of several combinations of in or between-row applications of different rates of CO2-emitting capsules and/or soil insecticides (here tefluthrin) aimed at preventing root damage by the pest larvae under field conditions. CO2 emission of the capsules in the soil lasted up to 28 days with a peak after 21 days coinciding with the first larval hatch. The pest density in the soil was not high enough to cause root damage above the economic threshold. Furthermore all tefluthrin applications, regardless of whether at full, half or quarter rates effectively prevented root damage; thus CO2 did not significantly further increase this efficacy. In-row applications of tefluthrin with or without CO2-emitting capsules prevented root damage to a much larger extent (59–77 % on the node injury scale) than the between-row applications of tefluthrin with or without capsules (17–31 %). In conclusion, further research on belowground orientation and movement of D. v. virgifera larvae, as well as tests with combinations of CO2-emitting capsules and lower rates of soil insecticide are needed to potentially develop attract and kill strategies as a management option against this maize pest.

Keywords

Western corn rootworm Carbon dioxide Tefluthrin Attract and kill Below ground interaction Zea mays 

Notes

Acknowledgments

This work was possible due to the technical support of the Plant Protection and Soil Conservation Directorate of Csongrad County in Hodmezovasarhely in Hungary, offered by Ibolya Hatala-Zseller, Laszlo Hodi and others. We like to thank the Cereal Research Station of Szeged and the Agroplanta RT for providing field space, Endre Szell and his team (Cereal Research Station of Szeged, Hungary) for technical support and field management, as well as our summer students Rajmond Stuber and Ferenc Koncz (Hodmezovasarhely, Hungary) and Nikolin Karapancsi (AGRINET Foundation, Korce, Albania) for their help in field work. We thank Stephan Dannert and Sebastian Fechner (FH Bielefeld, Germany) for the assistance in the production of CO2 capsules. This study was funded by Syngenta Crop Protection AG, Basel, Switzerland.

References

  1. Atterberg A (1905) Die rationelle Klassifikation der Sand und Kiese. Chemiker Zeitung 29:195–198Google Scholar
  2. Bermond G, Ciosi M, Lombaert E, Blin A, Boriani M, Furlan L, Toepfer S, Guillemaud T (2012) Secondary contact and admixture between independently invading populations of the western corn rootworm, Diabrotica virgifera virgifera in Europe. PLoS One 7:e50129PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bernklau EJ, Bjostad LB (1998a) Behavioral responses of first-instar western corn rootworm to carbon dioxide in a glass bead bioassay. J Econ Entomol 91:444–456Google Scholar
  4. Bernklau EJ, Bjostad LB (1998b) Reinvestigation of host location by western corn rootworm larvae (Coleoptera: Chrysomelidae): CO2 is the only volatile attractant. J Econ Entomol 91:1331–1340Google Scholar
  5. Bernklau EJ, Bjostad LB (2005) Insecticide enhancement with feeding stimulants in corn for western corn rootworm larvae (Coleoptera: Chrysomelidae). J Econ Entomol 98:1150–1156PubMedCrossRefGoogle Scholar
  6. Bernklau EJ, Fromm EA, Bjostad LB (2004) Disruption of host location of western corn rootworm larvae (Coleoptera: Chrysomelidae) with carbon dioxide. J Econ Entomol 97:330–339PubMedCrossRefGoogle Scholar
  7. Bernklau EJ, Bjostad LB, Meihls LN, Coudron TA, Lim E, Hibbard BE (2009) Localized search cues in corn roots for western corn rootworm (Coleoptera: Chrysomelidae) larvae. J Econ Entomol 102:558–562PubMedCrossRefGoogle Scholar
  8. Bernklau EJ, Bjostad LB, Hibbard BE (2011) Synthetic feeding stimulants enhance insecticide activity against western corn rootworm larvae, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). J Appl Entomol 135:47–54CrossRefGoogle Scholar
  9. Bidel LPR, Renault P, Pages L, Riviere LM (2001) An improved method to measure spatial variation in root respiration: application to the taproot of a young peach tree Prunus persica. Agronomie 21:179–192CrossRefGoogle Scholar
  10. Bjostad LB, Hibbard BE (1992) 6-Methoxy-2-benzoxazolinone: a semiochemical for host location by western corn rootworm larvae. J Chem Ecol 18:931–944PubMedCrossRefGoogle Scholar
  11. Boetel MA, Fuller BW, Evenson PD (2003) Emergence of adult northern and western corn rootworms (Coleoptera : Chrysomelidae) following reduced soil insecticide applications. J Econ Entomol 96:714–729PubMedCrossRefGoogle Scholar
  12. Chiang HC (1973) Bionomics of the northern and western corn rootworms. Annu Rev Entomol 18:47–72CrossRefGoogle Scholar
  13. Ciosi M, Miller NJ, Kim KS, Giordano R, Estoup A, Guillemaud T (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627PubMedCrossRefGoogle Scholar
  14. Ciosi M, Miller NJ, Toepfer S, Estoup A, Guillemaud T (2011) Stratified dispersal and increasing genetic variation during the invasion of Central Europe by the western corn rootworm, Diabrotica virgifera virgifera. Evol Appl 4:54–70PubMedCentralCrossRefGoogle Scholar
  15. Clark PL, Vaughn TT, Meinke LJ, Molina-Ochoa J, Foster JE (2006) Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) larval feeding behavior on transgenic maize (MON 863) and its isoline. J Econ Entomol 99:722–727PubMedCrossRefGoogle Scholar
  16. Cox WJ, Shields E, Cherney DJR (2008) Western corn rootworm damage subtly affects corn growth under moderate environmental stress. Crop Sci 48:1164–1169CrossRefGoogle Scholar
  17. Cressey D (2013) Reports spark row over bee-bothering insecticides. Nature News (16 January)Google Scholar
  18. Dunbar W, Gassmann AJ (2013) Abundance and distribution of western and northern corn rootworm (Diabrotica spp.) and prevalence of rotation resistance in eastern Iowa. J Econ Entomol 106:168–180PubMedCrossRefGoogle Scholar
  19. El-Sayed AM, Suckling DM, Byers JA, Jang EB, Wearing CH (2009) Potential of “lure and kill” in long-term pest management and eradication of invasive species. J Econ Entomol 102:815–835PubMedCrossRefGoogle Scholar
  20. European and Mediterranean Plant Protection Organization (EPPO) (2007) Efficacy evaluation of plant protection products: design and analysis of efficacy evaluation trials PP 1/152 (3). EPPO Bulletin 37Google Scholar
  21. European and Mediterranean Plant Protection Organization (EPPO) (2011) Evaluation of insecticides: Diabrotica v. virgifera. EPPO Standards for the efficacy evaluation of plant protection products PP1/212(2)Google Scholar
  22. Evenden ML, McLaughlin JR (2004) Factors influencing the effectiveness of an attracticide formulation against the Oriental fruit moth, Grapholita molesta. Entomol Exp Appl 112:89–97CrossRefGoogle Scholar
  23. Foster SP, Harris MO (1997) Behavioral manipulation methods for insect pest-management. Annu Rev Entomol 42:123–146PubMedCrossRefGoogle Scholar
  24. Fuller BW, Boetel MA, Walgenbach DD, Grundler JA, Hein GL, Jarvi KJ, Keaster AJ, Landis DA, Meinke LJ, Oleson JD, Ostlie KR, Tollefson JJ, Wedberg JL, Wilde GE, Evenson PD (1997) Optimization of soil insecticide rates for managing corn rootworm (Coleoptera: Chrysomelidae) larvae in the north central United States. J Econ Entomol 90:1332–1340Google Scholar
  25. Furlan L, Canzi S, Di Bernardo A, Edwards CR (2006) The ineffectiveness of insecticide seed coatings and planting-time soil insecticides as Diabrotica virgifera virgifera LeConte population suppressors. J Appl Entomol 130:485–490CrossRefGoogle Scholar
  26. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW (2011) Field-evolved resistance to Bacillus thuringiensis maize by western corn rootworm. PLoS One 6:e22629PubMedCentralPubMedCrossRefGoogle Scholar
  27. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW (2012) Western corn rootworm and Bacillus thuringiensis maize: challenges of pest resistance in the field. GM Crops Food 3:235–244PubMedCrossRefGoogle Scholar
  28. Gavloski JE, Whitfield GH, Ellis CR (1992) Effect of larvae of western corn rootworm (Coleoptera: Chrysomelidae) and of mechanical root pruning on sap flow and growth of corn. J Econ Entomol 85:1434–1441Google Scholar
  29. Girolami V, Marzaro M, Vivan L, Mazzon L, Greatti M, Giorio C, Marton D, Tapparo A (2012) Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implication. J Appl Entomol 136:17–26CrossRefGoogle Scholar
  30. Girolami V, Marzaro M, Vivan L, Mazzon L, Greatti M, Giorio C, Marton D, Tapparo A (2013) Aerial powdering of bees inside mobile cages and the extent of neonicotinoid cloud surrounding corn drillers. J Appl Entomol 137:35–44CrossRefGoogle Scholar
  31. Gould F (1991) Arthropod behaviour and the efficacy of plant protectants. Annu Rev Entomol 36:305–330CrossRefGoogle Scholar
  32. Goulson D (2013) An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50:977–987CrossRefGoogle Scholar
  33. Harris CR (1972) Factors influencing the effectiveness of soil insecticides. Annu Rev Entomol 17:177–198CrossRefGoogle Scholar
  34. Heuskin S, Verheggen FJ, Haubruge E, Wathelet JP, Lognay G (2011) The use of semiochemical slow-release devices in integrated pest management strategies. Biotechnol Agron Soc Environ 15:459–470Google Scholar
  35. Hibbard BE, Bernklau EJ, Bjostad LB (1994) Long-chain free fatty acids: semiochemicals for host location by western corn rootworm larvae. J Chem Ecol 20:3335–3344PubMedCrossRefGoogle Scholar
  36. Hiltpold I, Hibbard BE, French BW, Turlings TCJ (2012) Capsules containing entomopathogenic nematodes as a Trojan horse approach to control the western corn rootworm. Plant Soil 358:10–24CrossRefGoogle Scholar
  37. IUSS (2007) World reference base for soil resources. World resource reports, vol 103. FAO, RomeGoogle Scholar
  38. Johnson SN, Gregory PJ (2006) Chemically-mediated host-plant location and selection by root-feeding insects. Physiol Entomol 31:1–13CrossRefGoogle Scholar
  39. Johnson SN, Nielsen UN (2012) Foraging in the dark-chemically mediated host plant location by belowground insect herbivores. J Chem Ecol 38:604–614PubMedCrossRefGoogle Scholar
  40. Johnson SN, Zhang XX, Crawford JW, Gregory PJ, Hix NJ, Jarvis SC, Murray PJ, Young IM (2006) Effects of carbon dioxide on the searching behaviour of the root-feeding clover weevil Sitona lepidus (Coleoptera: Curculionidae). Bull Entomol Res 96:361–366PubMedGoogle Scholar
  41. Kahler AL, Olness AE, Sutter GR, Dybing CD, Devine OJ (1985) Root damage by western corn rootworm and nutrient in maize. Agron J 77:769–774CrossRefGoogle Scholar
  42. Kiss J, Edwards CR, Berger HK, Cate P, Cean M, Cheek S, Derron J, Festić H, Furlan L, Igrc-Barčić J, Ivanova I, Lammers W, Omelyuta V, Princzinger G, Reynaud P, Sivcev I, Sivicek P, Urek G, Vahala O (2005) Monitoring of western corn rootworm (Diabrotica virgifera virgifera LeConte) in Europe 1992–2003. In: Vidal S, Kuhlmann U, Edwards CR (eds) Western corn rootworm: ecology and management. CABI, Wallington, pp 29–41CrossRefGoogle Scholar
  43. Kriticos DJ, Reynaud P, Baker RHA, Eyre D (2012) Estimating the global area of potential establishment for the western corn rootworm (Diabrotica virgifera virgifera) under rain-fed and irrigated agriculture. Bull OEPP/EPPO Bull 42:56–64CrossRefGoogle Scholar
  44. Krysan JL (1986) Introduction: biology, distribution and identification of pest Diabrotica. In: Krysan JL, Miller AM (eds) Methods for the study of pest Diabrotica. Springer, New York, pp 1–23CrossRefGoogle Scholar
  45. Kuzyakov Y, Larionova AA (2005) Root and rhizomicrobial respiration: a review of approaches to estimate respiration by autotrophic and heterotrophic organisms in soil. J Plant Nutr Soil Sci 168:503–520CrossRefGoogle Scholar
  46. Lancashire PD, Bleiholder H, Vandenboom T, Langeluddeke P, Stauss R, Weber E, Witzenberger A (1991) A uniform decimal code for growth-stages of crops and weeds. Ann Appl Biol 119:561–601CrossRefGoogle Scholar
  47. Levine E, Oloumi-Sadeghi H (1991) Management of diabroticite rootworms in corn. Annu Rev Entomol 36:229–255CrossRefGoogle Scholar
  48. Mayo ZB (1986) Field evaluation of insecticides for control of larvae of corn rootworm. In: Krysan JL, Miller TA (eds) Methods for the study of pest Diabrotica. Springer, New York, pp 183–204CrossRefGoogle Scholar
  49. Mayo ZB, Peters LL (1978) Planting vs cultivation time applications of granular soil insecticides to control larvae of corn rootworms (Coleoptera: Chrysomelidae) in Nebraska. J Econ Entomol 71:801–803Google Scholar
  50. Miller N, Estoup A, Toepfer S, Bourguet D, Lapchin L, Derridj S, Seok Kim K, Renaud P, Furlan L, Guillemaud T (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310:992PubMedCrossRefGoogle Scholar
  51. Moellenbeck DJ, Peters ML, Bing JW, Rouse JR, Higgins LS, Sims L, Nevshemal T, Marshall L, Ellis RT, Bystrak PG, Lang BA, Stewart JL, Kouba K, Sondag V, Gustafson V, Nour K, Xu DP, Swenson J, Zhang J, Czapla T, Schwab G, Jayne S, Stockhoff BA, Narva K, Schnepf HE, Stelman SJ, Poutre C, Koziel M, Duck N (2001) Insecticidal proteins from Bacillus thuringiensis protect corn from corn rootworms. Nat Biotechnol 19:668–672PubMedCrossRefGoogle Scholar
  52. Moeser J, Hibbard BE (2005) A Synopsis of the nutritional ecology of larvae and adults of Diabrotica virgifera virgifera (Le Conte) in the new and old world nouvelle cuisine for the invasive maize pest Diabrotica virgifera virgifera in Europe? In: Vidal S, Kuhlmann U, Edwards CR (eds) Western corn rootworm: ecology and management. CABI, Wallington, pp 41–65CrossRefGoogle Scholar
  53. Oleson JD, Park YL, Nowatzki TM, Tollefson JJ (2005) Node-injury scale to evaluate root injury by corn rootworms (Coleoptera: Chrysomelidae). J Econ Entomol 98:1–8PubMedCrossRefGoogle Scholar
  54. Patel AV, Vorlop KD (1994) Entrapment of biological control agents applied to entomopathogenic nematodes. Biotechnol Tech 8:569–574CrossRefGoogle Scholar
  55. Pilz C, Keller S, Kuhlmann U, Toepfer S (2009) Comparative efficacy assessment of fungi, nematodes and insecticides to control western corn rootworm larvae in maize. Biocontrol 54:671–684CrossRefGoogle Scholar
  56. Pline M, Dusenbery DB (1987) Responses of plant parasitic nematode Meloidogyne incognita to carbon dioxide determined by video camera computer tracking. J Chem Ecol 13:873–888PubMedCrossRefGoogle Scholar
  57. Poullot D, Beslay D, Bouvier JC, Sauphanor B (2001) Is attract-and-kill technology potent against insecticide-resistant Lepidoptera? Pest Manag Sci 57:729–736PubMedCrossRefGoogle Scholar
  58. Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737PubMedCrossRefGoogle Scholar
  59. Robert CAM, Erb M, Duployer M, Zwahlen C, Doyen GR, Turlings TCJ (2012a) Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytol 194:1061–1069PubMedCrossRefGoogle Scholar
  60. Robert CAM, Erb M, Hibbard BE, French BW, Zwahlen C, Turlings TCJ (2012b) A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner. Funct Ecol 26:1429–1440CrossRefGoogle Scholar
  61. Schumann M, Vidal S (2012) Dispersal and spatial distribution of western corn rootworm larvae in relation to root phenology. Agric For Entomol 14:331–339CrossRefGoogle Scholar
  62. Schumann M, Patel A, Vemmer M, Vidal S (2013a) The role of carbon dioxide as an orientation cue for western corn rootworm larvae within the maize root system: implications for an attract-and-kill approach. Pest Manag Sci. doi: 10.1002/ps.3602 PubMedGoogle Scholar
  63. Schumann M, Patel A, Vidal S (2013b) Evaluation of an attract and kill strategy for western corn rootworm larvae. Appl Soil Ecol 64:178–189CrossRefGoogle Scholar
  64. Short DE, Luedtke RJ (1970) Larval migration of western corn rootworm. J Econ Entomol 63:325–326Google Scholar
  65. Singh P, Moore RF (1985) Handbook of insect rearing. Elsevier, AmsterdamGoogle Scholar
  66. Spencer JL, Hibbard BE, Moeser J, Onstad DW (2009) Behaviour and ecology of the western corn rootworm (Diabrotica virgifera virgifera LeConte). Agric For Entomol 11:9–27CrossRefGoogle Scholar
  67. Spike BP, Tollefson JJ (1991) Yield response of corn subjected to western corn rootworm (Coleoptera: Chrysomelidae) infestation and lodging. J Econ Entomol 84:1585–1590Google Scholar
  68. Strnad SP, Bergman MK (1987) Distribution and orientation of western corn rootworm (Coleoptera: Chrysomelidae) larvae in corn roots. Environ Entomol 16:1193–1198Google Scholar
  69. Strnad SP, Dunn PE (1990) Host search behavior of neonate western corn rootworm (Diabrotica virgifera virgifera). J Insect Physiol 36:201–205CrossRefGoogle Scholar
  70. Strnad SP, Bergman MK, Fulton WC (1986) First instar western corn rootworm (Coleoptera: Chrysomelidae) response to carbon dioxide. Environ Entomol 15:839–842Google Scholar
  71. Sutter GR, Branson TF, Fisher JR, Elliott NC, Jackson JJ (1989) Effect of insecticide treatments on root damage ratings of maize in controlled infestations of western corn rootworms (Coleoptera: Chrysomelidae). J Econ Entomol 82:1792–1798Google Scholar
  72. Sutter GR, Fisher JR, Elliott NC, Branson TF (1990) Effect of insecticide treatments on root lodging and yields of maize in controlled infestations of western corn rootworms (Coleoptera: Chrysomelidae). J Econ Entomol 83:2414–2420Google Scholar
  73. Toepfer S, Kuhlmann U (2006) Constructing life-tables for the invasive maize pest Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) in Europe. J Appl Entomol 130:193–205CrossRefGoogle Scholar
  74. Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:47–56CrossRefGoogle Scholar
  75. Vemmer M, Patel A (2011) Development of CO2 releasing beads to control soil borne insect pest. Paper presented at the 19th international conference on bioencapsulation, Amboise, FranceGoogle Scholar
  76. Villani MG, Wright RJ (1990) Environmetal influences on soil macroarthropod behavior in agricultural systems. Annu Rev Entomol 35:249–269CrossRefGoogle Scholar
  77. Wesseler J, Fall EH (2010) Potential damage costs of Diabrotica virgifera virgifera infestation in Europe: the ‘no control’ scenario. J Appl Entomol 134:385–394CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • M. Schumann
    • 1
    Email author
  • S. Toepfer
    • 2
    • 3
  • M. Vemmer
    • 4
  • A. Patel
    • 4
  • U. Kuhlmann
    • 3
  • S. Vidal
    • 1
  1. 1.Department of Crop Sciences, Agricultural EntomologyGeorg-August UniversityGöttingenGermany
  2. 2.CABI c/o Plant Protection DirectorateHodmezovasarhelyHungary
  3. 3.CABI Europe - SwitzerlandDelémontSwitzerland
  4. 4.Department of Engineering and MathematicsUniversity of Applied Sciences, Engineering and Alternative Fuels, BielefeldBielefeldGermany

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