Abstract
The behavior of the neonate larvae of the western corn rootworm (WCR) Diabrotica virgifera virgifera LeConte, a major pest of maize, was assessed in the presence of maize roots constitutively emitting (E)-β-caryophyllene (EβC). This root volatile has been shown to attract both second instar WCR and insect-killing nematodes, and may offer innovative alternatives in helping to manage WCR. Under greenhouse conditions, the maize inbred line HiII, lacking the ability to emit EβC, was planted 75 cm from the maize inbred line 201-L1, the HiII inbred genetically engineered to constitutively emit EβC. WCR eggs were infested in the center of the two lines and neonate attraction toward either root system was recorded after collecting WCR larvae established on the plants. Whereas marginally more larvae were found on EβC-emitting plants, counts of recovered WCR neonates did not significantly differ between the two lines. This supports the postulate that CO2 is the primary attractant for WCR neonate larvae. The chemical ecology of WCR larvae is discussed. A conceptual model of the foraging behavior of this pest is proposed, summarizing our current knowledge on chemically mediated interactions between WCR larvae and maize roots.
References
Bermond G, Ciosi M, Lombaert E et al (2012) Secondary contact and admixture between independently invading populations of the western corn rootworm, Diabrotica virgifera virgifera in Europe. PLoS One 7:e50129
Bernklau EJ, Bjostad LB (1998a) Re-investigation of host location by western corn rootworm larvae (Coleoptera: Chrysomelidae): CO2 is the only volatile attractant. J Econ Entomol 91:1331–1340
Bernklau EJ, Bjostad LB (1998b) Behavioral responses of first instar western corn rootworm (Coleoptera: Chrysomelidae) to CO2 in a glass bead bioassay. J Econ Entomol 91:444–456
Bernklau EJ, Bjostad LB (2005) Insecticide enhancement with feeding stimulants in corn for western corn rootworm larvae (Coleoptera: Chrysomelidae). J Econ Entomol 98:1150–1156
Bernklau EJ, Bjostad LB (2008) Identification of feeding stimulants in corn roots for western corn rootworm larvae (Coleoptera: Chrysomelidae). J Econ Entomol 101:341–351
Bernklau EJ, Fromm EA, Bjostad LB (2004) Disruption of host location of western corn rootworm larvae (Coleoptera: Chrysomelidae) with carbon dioxide. J Econ Entomol 97:330–339
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 135:47–54
Bernklau E, Hibbard BE, Bjostad LB (2013) Isolation and characterization of host recognition cues in corn roots for larvae of the western corn rotworm (Coleptera: Chrysomelidae). J Econ Entomol 106:2354–2363
Bernklau EJ, Hibbard BE, Dick DL, Rithner CD, Bjostad LB (2015) Monogalactosyldiacylglycerols as host recognition cues for western corn rootworm larvae (Coleoptera: Chrysomelidae). J Econ Entomol 108:539–548
Bjostad LB, Hibbard BE (1992) 6-Methoxy-2-benzoxalinone-a semiochemical for host location by western corn-rootworm larvae. J Chem Ecol 18:931–944
Branson TF (1982) Olfactory response of larvae of Diabrotica virgifera virgifera to plant roots. Entomol Exp Appl 31:303–307
Ciosi M, Miller NJ, Kim KS et al (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: Multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627
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 4:54–70
Degenhardt J, Hiltpold I, Köllner TG et al (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci USA 106:13213–13218
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 102:815–835
Erb M, Huber M, Robert CAM et al (2013) The role of plant primary and secondary metabolites in root-herbivore behaviour, nutrition and physiology. In: Johnson SN, Hiltpold I, Turlings TCJ (eds) Advances in insect physiology, vol 45. Academic Press, Oxford, pp 53–95
Hibbard BE, Bjostad LB (1988) Behavioral response of westrn corn rootworm larvae to volatile semiochemiclas from corn seedlings. J Chem Ecol 14:1523–1539
Hibbard BE, Bjostad LB (1989) Corn semiochemicals and their effects on insecticide efficacy and insecticide repellency toward western corn rootworm larave (Coleoptera: Chrysomelidae). J Econ Entomol 82:773–781
Hibbard BE, Bernklau EJ, Bjostad LB (1994) Long-chain free fatty-acids: semiochemicals for host location by western corn rooworm larvae. J Chem Ecol 20:3335–3344
Hibbard BE, Peairs FB, Pilcher SD et al (1995) Germinating corn extracts and 6-methoxy-2-benzoxazolinone—western corn-rootworm (Coeiptera, Chrysomelidae) larval attractants evaluated with soil insecticides 88, pp 716–724
Hibbard BE, Duran DP, Ellersieck MR, Ellsbury MM (2003) Post-establishment movement of western corn rootworm larvae (Coleoptera: Chrysomelidae) in Central Missouri corn. J Econ Entomol 96:599–608
Hibbard BE, Higdon ML, Duran DP, Schweikert YM, Ellersieck MR (2004) Role of egg density on establishment and plant-to-plant movement by western corn rootworm larvae (Coleoptera: Chrysomelidae). J Econ Entomol 97:871–882
Hibbard BE, Schweikert YM, Higdon ML, Ellersieck MR (2008) Maize phenology affects establishment, damage, and development of the western corn rootworm (Coleoptera: Chrysomelidae). Environ Entomol 37:1558–1564
Hibbard BE, Meihls LN, Ellersieck MR, Onstad DW (2010) Density-dependent and density-independent mortality of the western corn rootworm: impact on dose calculations of rootworm-resistant Bt corn. J Econ Entomol 103:77–84
Hiltpold I, Turlings TCJ (2008) Belowground chemical signalling in maize: when simplicity rhymes with efficiency. J Chem Ecol 34:628–635
Hiltpold I, Turlings TCJ (2012) Manipulation of chemically mediated interactions in agricultural soils to enhance the control of crop pests and to improve crop yield. J Chem Ecol 38:641–650
Hiltpold I, Toepfer S, Kuhlmann U, Turlings TCJ (2010) How maize root volatiles influence the efficacy of entomopathogenic nematodes against the western corn rootworm? Chemoecology 20:155–162
Hiltpold I, Hibbard BE, French DW, Turlings TCJ (2012) Capsules containing entomopathogenic nematodes as a Trojan horse approach to control the western corn rootworm. Plant Soil 358:11–25
Hiltpold I, Bernklau E, Bjostad LB et al (2013) Nature, evolution and characterisation of rhizospheric chemical exudates affecting root herbivores. In: Johnson SN, Hiltpold I, Turlings TCJ (eds) Advances in insect physiology, vol 45. Academic Press, Oxford, pp 97–157
Jackson JJ (1985) Diabrotica spp. In: Moore RF (ed) Handbook of insect rearing, vol I., ElsevierNew York, NY, pp 237–254
Johnson SN, Gregory PJ (2006) Chemically-mediated host-plant location and selection by root-feeding insects. Physiol Entomol 31:1–13
Johnson SN, Nielsen UN (2012) Foraging in the dark-chemically mediated host plant location by belowground insect herbivores. J Chem Ecol 38:604–614
Khan ZR, AmpongNyarko K, Chiliswa P et al (1997) Intercropping increases parasitism of pests. Nature 388:631–632
Köllner TG, Held M, Lenk C et al (2008) A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20:482–494
Miller N, Estoup A, Toepfer S et al (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310:992
Mitchell P (2011) Costs and benefits of controlling pest Diabrotica in maize in the United States. Paper presented at the 24th IWGO Conference, Freiburg, Germany, 24–26 Oct. 2011
Moeser J, Hibbard BE (2005) A synopsis of the nutritional ecology of larvae and adults of Diabrotica virgifera virgifera (LeConte) in the New and Old World—Nouvelle cuisine for the invasive maize pest Diabrotica virgifera virgifera in Europe? In: Vidal S, Kuhlmann U, Edwards R (eds) Western corn rootworm: ecology and management. CABI Publishers, Wallingford, pp 45–61
Pike DR, Steffey KL, Gray ME et al (1995) Biological and economic assessment of pesticide use on corn and soybeans. USDA-National Agricultural Pesticide Impact Assessment Program, Washington
Rasmann S, Köllner TG, Degenhardt J et al (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737
Robert CAM, Erb M, Duployer M et al (2012a) Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytol 194:1061–1069
Robert CAM, Erb M, Hibbard BE et al (2012b) A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner. Funct Ecol 26:1429–1440
Robert CAM, Veyrat N, Glauser G et al (2012c) A specialist root herbivore takes advantage of defensive metabolites to locate nutritious tissues. Ecol Lett 15:55–64
Santos F, Peñaflor MFGV, Paré PW et al (2014) A novel interaction between plant-beneficial rhizobacteria and roots: colonization induces corn resistance against the root herbivore. Diabrotica Speciosa 9:e113280
Schumann M, Patel A, Vidal S (2013) Evaluation of an attract and kill strategy for western corn rootworm larvae. Appl Soil Ecol 64:178–189
Schumann M, Patel A, Vemmer M, Vidal S (2014a) 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 70:642–650
Schumann M, Patel A, Vidal S (2014b) Soil application of an encapsulated CO2 source and its potential for management of western corn rootworm larvae. J Econ Entomol 107:230–239
Schumann M, Toepfer S, Vemmer M et al (2014c) Field evaluation of an attract and kill strategy against western corn rootworm larvae, pp 1–13
Strnad SP, Bergman MK (1987) Distribution and orientation of western corn-rootworm (Coleoptera, Chrysomelidae) larvae in corn roots 16, pp 1193–1198
Strnad SP, Dunn PE (1990) Host search behavior of neonate western corn rootworm (Diabrotica virgifera virgifera). J Econ Entomol 36:201–205
Strnad SP, Bergman MK, Fulton WC (1986) First-instar western corn rootworm (Coleoptera: Chrysomelidae) response to carbon dioxide. Environ Entomol 15:839–842
Szalai M, Komáromi JP, Bažok R et al (2011) Generational growth rate estimates of Diabrotica virgifera virgifera populations (Coleoptera: Chrysomelidae) J. Pest Sci 84:133–142
Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 359:51–60
Turner SL, Li N, Guda T et al (2011) Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes. Nature 474:87–91
Urias-Lopez M, Meinke LJ, Higley LG, Haile FJ (2000) Influence of western corn rootworm (Coleoptera: Chrysomelidae) larval injury on photosynthetic rate and vegetative growth of different types of maize. Environ Entomol 29:861–867
Wesseler J, Fall EH (2010) Potential damage costs of Diabrotica virgifera virgifera infestation in Europe-the ‘no control’ scenario. J Appl Entomol 134:385–394
Acknowledgments
The authors thank Prof. J. Degenhardt (Martin-Luther-Universität Halle-Wittenberg, Germany) for the maize seeds used in the reported experiments. The authors acknowledge the constructive comments made by the reviewers. Funding for this project was provided by the Swiss National Science Foundation (SNSF) Grant No. PBNEP3-134385 awarded to I. Hiltpold.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Traugott.
Rights and permissions
About this article
Cite this article
Hiltpold, I., Hibbard, B.E. Neonate larvae of the specialist herbivore Diabrotica virgifera virgifera do not exploit the defensive volatile (E)-β-caryophyllene in locating maize roots. J Pest Sci 89, 853–858 (2016). https://doi.org/10.1007/s10340-015-0714-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-015-0714-7