Skip to main content
Log in

Foraging in the Dark – Chemically Mediated Host Plant Location by Belowground Insect Herbivores

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Root-feeding insects are key components in many terrestrial ecosystems. Like shoot-feeding insect herbivores, they exploit a range of chemical cues to locate host plants. Respiratory emissions of carbon dioxide (CO2) from the roots is widely reported as the main attractant, however, there is conflicting evidence about its exact role. CO2 may act as a ‘search trigger’ causing insects to search more intensively for more host specific signals, or the plant may ‘mask’ CO2 emissions with other root volatiles thus avoiding detection. At least 74 other compounds elicit behavioral responses in root-feeding insects, with the majority (>80 %) causing attraction. Low molecular weight compounds (e.g., alcohols, esters, and aldehydes) underpin attraction, whereas hydrocarbons tend to have repellent properties. A range of compounds act as phagostimulants (e.g., sugars) once insects feed on roots, whereas secondary metabolites often deter feeding. In contrast, some secondary metabolites usually regarded as plant defenses (e.g., dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA)), can be exploited by some root-feeding insects for host location. Insects share several host location cues with plant parasitic nematodes (CO2, DIMBOA, glutamic acid), but some compounds (e.g., cucurbitacin A) repel nematodes while acting as phagostimulants to insects. Moreover, insect and nematode herbivory can induce exudation of compounds that may be mutually beneficial, suggesting potentially significant interactions between the two groups of herbivores. While a range of plant-derived chemicals can affect the behavior of root-feeding insects, little attempt has been made to exploit these in pest management, though this may become a more viable option with diminishing control options.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
€32.70 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Finland)

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ali, J. G., Alborn, H. T., and Stelinski, L. L. 2011. Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J. Ecol. 99:26–35.

    CAS  Google Scholar 

  • Andersen, D. C. 1987. Belowground herbivory in natural communities—a review emphasizing fossorial animals. Q. Rev. Biol. 62:261–286.

    Google Scholar 

  • Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., and Vivanco, J. M. 2006. The role of root exudates in rhizosphere interations with plants and other organisms. Annu. Rev. Plant Biol. 57:233–266.

    PubMed  CAS  Google Scholar 

  • Bernays, E. A. and Chapman, R. F. 1994. Host-Plant Selection by Phytophagous Insects. Chapman & Hall, New York.

    Google Scholar 

  • Bernays, E. A. and Woodhead, S. 1982. Plant phenols utilized as nutrients by a phytophagous insect. Science 216:201–203.

    PubMed  CAS  Google Scholar 

  • Bernays, E. A., Chamberlain, D. J., and Woodhead, S. 1983. Phenols as nutrients for a phytophagous insect Anacridium melanorhodon. J. Insect Physiol. 29:535–539.

    CAS  Google Scholar 

  • Bernklau, E. J. and Bjostad, L. B. 1998a. Behavioral responses of first-instar western corn rootworm (Coleoptera: Chrysomelidae) to carbon dioxide in a glass bead bioassay. J. Econ. Entomol. 91:444–456.

    Google Scholar 

  • Bernklau, E. J. and Bjostad, L. B. 1998b. Reinvestigation of host location by western corn rootworm larvae (Coleoptera: Chrysomelidae): CO2 is the only volatile attractant. J. Econ. Entomol. 91:1331–1340.

    Google Scholar 

  • Bernklau, E. J., Fromm, E. A., and Bjostad, L. B. 2004. Disruption of host location of western corn rootworm larvae (Coleoptera: Chrysomelidae) with carbon dioxide. J. Econ. Entomol. 97:330–339.

    PubMed  CAS  Google Scholar 

  • Bird, A. F. 1959. The attractiveness of roots to the plant parasitic nematodes Meloidogyne javanica and M. hapla. Nematologica 4:322–335.

    Google Scholar 

  • Bird, A. F. 1962. Orientation of the larvae of Meloidogyne javanica relative to roots. Nematologica 7:275–287.

    Google Scholar 

  • Bjostad, L. B. and Hibbard, B. E. 1992. 6-methoxy-2-benzoxazolinone—a semiochemical for host location by western corn rootworm larvae. J. Chem. Ecol. 18:931–944.

    CAS  Google Scholar 

  • Blackshaw, R. P. and Kerry, B. R. 2008. Root herbivory in agricultural ecosystems, pp. 35–53, in S. N. Johnson and P. J. Murray (eds.), Root Feeders—An Ecosystem Perspective. CABI, Wallingford.

    Google Scholar 

  • Britton, E. B. 1978. Revision of Australian chafers (Coleoptera: Scarabaeidae: Melolonthinae) vol. 2 tribe Melolonthini. Aust. J. Zool. (supp). 60:1–150.

  • Calkins, C. O., Matteson, J. W., and Randall, D. D. 1967. Response of false wireworm Eleodes suturalis larvae to wheat in olfactometer tests. J. Econ. Entomol. 60:665–668.

    Google Scholar 

  • Chapman, R. F. 2003. Contact chemoreception in feeding by phytophagous insects. Annu. Rev. Entomol. 48:455–484.

    PubMed  CAS  Google Scholar 

  • Chitwood, D. J. 2002. Phytochemical based strategies for nematode control. Annu. Rev. Phytopathol. 40:221–249.

    PubMed  CAS  Google Scholar 

  • Cipollini, D., Rigsby, C., and Barto, E. K. 2012. Soil microbes as targets and mediators of allelopathy in plants. J. Chem. Ecol. 38: ------ this issue.

  • Clark, K. E., Hartley, S. E., and Johnson, S. N. 2011. Does mother know best? Parent-offspring conflict in aboveground-belowground herbivore lifecycles. Ecol. Entomol. 36:117–124.

    Google Scholar 

  • Clark, K. E., Hartley, S. E., Brennan, R. M., Jennings, S. N., McMenemy, L. S., McNicol, J. W., Mitchell, C., and Johnson, S. N. 2012. Effects of cultivar and egg density on a colonizing vine weevil (Otiorhynchus sulcatus) population and its impacts on red raspberry growth and yield. Crop Prot. 32:76–82.

    Google Scholar 

  • Clemens, C. D., Aumann, J., Spiegel, Y., and Wyss, U. 1994. Attractant-mediated behavior of mobile stages of Heterodera schachtii. Fund. Appl. Nematol. 17:569–574.

    Google Scholar 

  • de Deyn, G. B., Raaijmakers, C. E., Zoomer, H. R., Berg, M. P., de Ruiter, P. C., Verhoef, H. A., Bezemer, T. M., and van der Putten, W. H. 2003. Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713.

    PubMed  Google Scholar 

  • Doane, J. F., Lee, Y. W., Westcott, N. D., and Klingler, J. 1975. The orientation response of Ctenicera destructor and other wireworms (Coleoptera: Elateridae) to germinating grain and to carbon dioxide. Can. Entomol. 107:1233–1251.

    Google Scholar 

  • Dobler, S., Petschenka, G., and Pankoke, H. 2011. Coping with toxic plant compounds—the insect’s perspective on iridoid glycosides and cardenolides. Phytochemistry 72:1593–1604.

    PubMed  CAS  Google Scholar 

  • Dusenbery, D. B. 1987. Theoretical range over which bacteria and nematodes locate plant roots using carbon dioxide. J. Chem. Ecol. 13:1617–1624.

    Google Scholar 

  • Eben, A., Barbercheck, M. E., and Aluja, M. 1997. Mexican diabroticite beetles. 1. Laboratory test on host breadth of Acalymma and Diabrotica spp. Entomol. Exp. Appl. 82:53–62.

    Google Scholar 

  • Effmert, U., Kalderas, J., Warnke, R., and Piechulla, B. 2012. Volatile mediated interactions between bacteria and fungi in the soil. J. Chem. Ecol. 38: ------ this issue.

  • Finch, S. and Skinner, G. 1974. Studies of the cabbage root fly, pp. 84–85, in: Report of National Vegetable Research Station, 1973. National Vegetable Research Station, Wellesbourne.

  • Friebe, A., Klever, W., Sikora, R., and Schnabl, H. 1998. Allelochemicals in root exudates of maize: effects on root lesion nematode Pratylenchus zeae, pp. 71–93, in J. T. Romeo, K. R. Downum, and R. Verpoorte (eds.), Phytochemical Signals and Plant-Microbe Interactions. Recent Advances in Phytochemistry Vol. 32. Plenum Press, New York.

    Google Scholar 

  • Galbreath, R. A. 1988. Orientation of grass grub Costelytra zealandica (Coleoptera: Scarabaeidae) to a carbon dioxide source. N. Z. Entomol. 11:6–7.

    Google Scholar 

  • Gaynor, D. L., Lane, G. A., Biggs, D. R., and Sutherland, O. R. W. 1986. Measurement of grass grub resistance of bean in a controlled environment. N. Z. J. Exp. Agric. 14:77–82.

    Google Scholar 

  • Gerard, P. J. 2001. Dependence of Sitona lepidus (Coleoptera: Curculionidae) larvae on abundance of white clover Rhizobium nodules. Bull. Entomol. Res. 91:149–152.

    PubMed  CAS  Google Scholar 

  • Grayston, S. J., Dawson, L. A., Treonis, A. M., Murray, P. J., Ross, J., Reid, E. J., and MacDougall, R. 2001. Impact of root herbivory by insect larvae on soil microbial communities. Eur. J. Soil Biol. 37:277–280.

    CAS  Google Scholar 

  • Gregory, P. J. 2006. Plant Roots—Growth, Activity and Interaction with Soils. Blackwell Publishing, Oxford.

    Google Scholar 

  • Guerin, P. M. and Ryan, M. F. 1984. Relationship between root volatiles of some carrot cultivars and their resistance to the carrot fly, Psila rosae. Entomol. Exp. Appl. 36:217–224.

    CAS  Google Scholar 

  • Hamilton, C. C. 1917. The behaviour of some soil insects in gradients of evaporating powder of air, carbon dioxide and ammonia. Biol. Bull. 32:159–182.

    CAS  Google Scholar 

  • Hartmann, A. and Schikora, A. 2012. Quorum sensing of bacteria and trans-kingdom interactions of N-acyl homoserine lactones with eukaryotes. J. Chem. Ecol. 38: ------ this issue.

  • Haynes, R. L. and Jones, C. M. 1976. Effects of the Bi locus in cucumber on reproduction, attraction, and response of the plant to infection by the southern rootknot nematode. J. Am. Soc. Hortic. Sci. 101:422–424.

    Google Scholar 

  • Hibbard, B. E., Bernklau, E. J., and Bjostad, L. B. 1994. Long-chain free fatty-acids—semiochemicals for host location by western corn rootworm larvae. J. Chem. Ecol. 20:3335–3344.

    CAS  Google Scholar 

  • Hiltpold, I. and Turlings, T. C. J. 2012. Manipulation of chemically mediated interactions in agricultural soils to enhance the control of crop pests. J. Chem. Ecol. 38: ------ this issue.

  • Horton, D. R. and Landolt, P. J. 2002. Orientation response of Pacific coast wireworm (Coleoptera: Elateridae) to food baits in laboratory and effectiveness of baits in field. Can. Entomol. 134:357–367.

    Google Scholar 

  • Huang, X. P. and Mack, T. P. 2001. Artificial carbon dioxide source to attract lesser cornstalk borer (Lepidoptera: Pyralidae) larvae. J. Econ. Entomol. 94:860–867.

    PubMed  CAS  Google Scholar 

  • Huang, X. P. and Mack, T. P. 2002. Collection and determination of lesser cornstalk borer (Lepidoptera: Pyralidae) larval attractant from peanut plants. Environ. Entomol. 31:15–21.

    Google Scholar 

  • Hunter, M. D. 2001. Out of sight, out of mind: The impacts of root-feeding insects in natural and managed systems. Agric. For. Entomol. 3:3–9.

    Google Scholar 

  • Ikeshoji, T., Ishikawa, Y., and Matsumoto, Y. 1980. Attractants against the onion maggots and flies, Hylemya antiqua, in onions inoculated with bacteria. J. Pestic. Sci. 5:343–350.

    CAS  Google Scholar 

  • Jewett, D. K. and Bjostad, L. B. 1996. Dichloromethane attracts diabroticite larvae in a laboratory behavioral bioassay. J. Chem. Ecol. 22:1331–1344.

    CAS  Google Scholar 

  • Johnson, S. N. and Gregory, P. J. 2006. Chemically-mediated host-plant location and selection by root-feeding insects. Physiol. Entomol. 31:1–13.

    CAS  Google Scholar 

  • Johnson, S. N. and McNicol, J. W. 2010. Elevated CO2 and aboveground-belowground herbivory by the clover root weevil. Oecologia 162:209–216.

    PubMed  Google Scholar 

  • Johnson, S. N. and Murray, P. J. (eds.) 2008. Root Feeders—An Ecosystem Perspective. CABI, Wallingford.

    Google Scholar 

  • Johnson, S. N., Gregory, P. J., Greenham, J. R., Zhang, X., and Murray, P. J. 2005. Attractive properties of an isoflavonoid found in white clover root nodules on the clover root weevil. J. Chem. Ecol. 31:2223–2229.

    PubMed  CAS  Google Scholar 

  • Johnson, S. N., Zhang, X. X., Crawford, J. W., Gregory, P. J., Hix, N. J., Jarvis, S. J., Murray, P. J., and Young, I. M. 2006. Effects of CO2 on the searching behaviour of the root-feeding clover weevil. Bull. Entomol. Res. 96:361–366.

    PubMed  CAS  Google Scholar 

  • Johnson, S. N., Hawes, C., and Karley, A. J. 2009. Reappraising the role of plant nutrients as mediators of interactions between root- and foliar-feeding insects. Funct. Ecol. 23:699–706.

    Google Scholar 

  • Johnson, S. N., Barton, A. T., Clark, K. E., Gregory, P. J., McMenemy, L. S., and Hancock, R. D. 2011. Elevated atmospheric carbon dioxide impairs the performance of root-feeding vine weevils by modifying root growth and secondary metabolites. Global Change Biol. 17:688–695.

    Google Scholar 

  • Jones, O. T. and Coaker, T. H. 1977. Orientated responses of carrot fly larvae, Psila rosae, to plant odours, carbon dioxide and carrot root volatiles. Physiol. Entomol. 2:189–197.

    CAS  Google Scholar 

  • Jones, O. T. and Coaker, T. H. 1978. A basis for host plant finding in phytophagous larvae. Entomol. Exp. Appl. 24:272–284.

    Google Scholar 

  • Jones, O. T. and Coaker, T. H. 1979. Responses of carrot fly larvae, Psila rosae, to the odorous and contact-chemostimulatory metabolites of host and non-host plants. Physiol. Entomol. 4:353–360.

    CAS  Google Scholar 

  • Jung, S. C., Martinez-Medina, A., Lopez Raez, J. A., and Pozo, M. J. 2012. Priming of plant defences in mycorrhiza-induced resistance. J. Chem. Ecol. 38: ------ this issue.

  • Kamm, J. A. and Buttery, R. G. 1984. Root volatile components of red clover—identification and bioassay with the clover root borer (Coleoptera, Scolytidae). Environ. Entomol. 13:1427–1430.

    CAS  Google Scholar 

  • Karban, R. 1980. Periodical cicada nymphs impose periodical oak tree wood accumulation. Nature 287:326–327.

    Google Scholar 

  • Klingler, J. 1957. Über die Bedeutung des Kohlendioxyds fur die Orientierung der Larven von Otiorrhynchus sulcatus F., Melolontha und Agriotes (Col.) im Boden (Vorläufige Mitteilung). Mitt. Schweiz. Entomol. Ges. 30:317–322.

    Google Scholar 

  • Klingler, J. 1958. Die Bedeutung der Kohlendioxyd-Ausscheidung der Wurzeln für die Orientierung der Larven von Otiorrhynchus sulcatus F. und anderer bodenbewohnender phytophager Insektenarten. Mitt. Schweiz. Entomol. Ges. 31:205–269.

    Google Scholar 

  • Klingler, J. 1961. Anziehungsversuche mit Ditylenchus dipsaci unter Berücksichtigung der wirkung des Kohlendioxyds, des Redoxpotentials und anderer Faktoren. Nematologica 6:69–84.

    CAS  Google Scholar 

  • Klingler, J. 1965. On the orientation of plant nematodes and of some other soil animals. Nematologica 11:4–18.

    Google Scholar 

  • Klingler, J. 1966. The location of the CO2 chemoreceptors in the larva of Otiorrhynchus sulcatus. Entomol. Exp. Appl. 9:271–277.

    Google Scholar 

  • Koštál, V. 1992. Orientation behavior of newly hatched larvae of the cabbage maggot, Delia radicum (L.) (Diptera, Anthomyiidae), to volatile plant metabolites. J. Insect Behav. 5:61–70.

    Google Scholar 

  • Lane, G. A., Biggs, D. R., Russell, G. B., Sutherland, O. R. W., Williams, E. M., Maindonald, J. H., and Donnell, D. J. 1985. Isoflavonoid feeding deterrents for Costelytra zealandica—structure-activity-relationships. J. Chem. Ecol. 11:1713–1735.

    CAS  Google Scholar 

  • Lees, A. D. 1943. On the behaviour of wireworms of the genus Agriotis Esch. (Coleoptera, Elateridae). I. Reactions to humidity. J. Exp. Biol. 20:43–53.

    Google Scholar 

  • Long, D. B. 1958. Host plant location by larvae of the wheat bulb fly (Leptohylemyia coarctata Fallén). Proc. Roy. Entomol. Soc. 33:1–8.

    Google Scholar 

  • Macdonald, P. J. and Ellis, C. R. 1990. Survival time of unfed, 1st instar western corn rootworm (Coleoptera, Chrysomelidae) and the effects of soil type, moisture, and compaction on their mobility in soil. Environ. Entomol. 19:666–671.

    Google Scholar 

  • Maki, A. and Ryan, M. F. 1989. Root-mediated effects in carrot resistance to the carrot fly, Psila rosae. J. Chem. Ecol. 15:1867–1882.

    Google Scholar 

  • Maki, A., Kitajima, J., Stewart, G., Abe, F., and Ryan, M. F. 1989. Isolation, identification, and bioassay of chemicals affecting nonpreference carrot root resistance to carrot-fly larvae. J. Chem. Ecol. 15:1883–1897.

    CAS  Google Scholar 

  • Mathesius, U. 2001. Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. J. Exp. Bot. 52:419–426.

    PubMed  CAS  Google Scholar 

  • Matsumoto, Y. 1970. Volatile organic sulfur compounds as insect attractants with special reference to host selection, pp. 133–160, in D. L. Wood, R. M. Silverstein, and M. Nakajima (eds.), Control of Insect Behavior by Natural Products. Academic, New York.

    Google Scholar 

  • Matsumoto, Y. and Thorsteinson, A. J. 1968. Olfactory response of larvae of the onion maggot, Hylemya antiqua Meigen (Diptera: Anthomyiidae) to organic sulfur compounds. Appl. Entomol. Zool. 3:107–111.

    Google Scholar 

  • Mochizuki, A., Ishikawa, Y., and Matsumoto, Y. 1989. Olfactory response of the larvae of the onion fly, Hylemya antiqua Meigen (Diptera: Anthomyiidae) to volatile compounds. Appl. Entomol. Zool. 24:29–35.

    Google Scholar 

  • Morgan, A. C. and Crumb, S. E. 1928. Notes on the chemotrophic responses of certain insects. J. Econ. Entomol. 21:913–920.

    Google Scholar 

  • Nordenhem, H. and Nordlander, G. 1994. Olfactory oriented migration through soil by root-living Hylobius abietis (L.) larvae (Col., Curculionidae). J. Appl. Entomol. 117:457–462.

    Google Scholar 

  • Payne, D. and Gregory, P. J. 1988. The soil atmosphere, pp. 298–314, in A. Wild (ed.), Russell’s Soil Conditions and Plant Growth. Longman, Harlow, U.K.

    Google Scholar 

  • Perry, R. N. 1997. Plant signals in nematode hatching and attraction, pp. 38–50, in C. Fenoll, F. M. W. Grundler, and S. A. Ohl (eds.), Cellular and Molecular Aspects of Plant-Nematode Interactions. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Perry, R. N. and Aumann, J. 1998. Behaviour and sensory responses, pp. 75–102, in R. N. Perry and D. J. Wright (eds.), The Physiology and Biochemistry of Free-Living and Plant-Parasitic Nematodes. CABI Publishing, Oxon.

    Google Scholar 

  • Prot, J. C. 1980. Migration of plant-parasitic nematodes toward plant roots. Revue de Nématologie 3:305–318.

    Google Scholar 

  • Rasmann, S., Ali, J., Helder, J., and Van Der Putten, W. H. 2012. Ecology and evolution of soil nematode chemotaxis. J. Chem. Ecol. 38: ------ this issue.

  • Reinecke, A., Mueller, F., and Hilker, M. 2008. Attractiveness of CO2 released by root respiration fades on the background of root exudates. Basic Appl. Ecol. 9:568–576.

    CAS  Google Scholar 

  • Riga, E., Perry, R. N., Barrett, J., and Johnston, M. R. L. 1997. Electrophysiological responses of male potato cyst nematodes, Globodera rostochiensis and G. pallida, to some chemicals. J. Chem. Ecol. 23:417–428.

    CAS  Google Scholar 

  • Robert, C. A. M., Veyrat, N., Glauser, G., Marti, G., Doyen, G. R., Villard, N., Gailland, M., Köllner, T., Giron, D., Body, M., Babst, B., Ferrieri, R., Turlings, T. C. J., and Erb, M. 2012. A specialist root herbivore exploits defensive metabolites to locate nutritious tissues. Ecol. Lett. 15:55–64.

    PubMed  Google Scholar 

  • Rogers, H. H., Runion, G. B., and Krupa, S. V. 1994. Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. Environ. Pollut. 83:155–189.

    PubMed  CAS  Google Scholar 

  • Rogers, H. H., Prior, S. A., Runion, G. B., and Mitchell, R. J. 1996. Root to shoot ratio of crops as influenced by CO2. Plant Soil 187:229–248.

    CAS  Google Scholar 

  • Ross, K. T. A. and Anderson, M. 1992. Larval responses of three vegetable root fly pests of the Genus Delia (Diptera, Anthomyiidae) to plant volatiles. Bull. Entomol. Res. 82:393–398.

    Google Scholar 

  • Rudinsky, J. A. 1966. Scolytid beetles associated with Douglas-fir: Responses to terpenes. Science 152:218–219.

    PubMed  CAS  Google Scholar 

  • Rudinsky, J. A. and Zethner-Møller, O. 1967. Olfactory responses of Hylastes nigrinus to various host materials. Can. Entomol. 99:911–916.

    Google Scholar 

  • Russell, G. B., Sutherland, O. R. W., Christmas, P. E., and Wright, H. 1982. Feeding deterrents for black beetle larvae, Heteronychus arator (Scarabaeidae), in Trifolium repens. N. Z. J. Zool. 9:145–149.

    Google Scholar 

  • Ryan, M. F. and Guerin, P. M. 1982. Behavioral responses of the carrot fly larva, Psila rosae, to carrot root volatiles. Physiol. Entomol. 7:315–324.

    CAS  Google Scholar 

  • Rygg, T. and Sömme, L. 1972. Oviposition and larval development of Hylemya floralis (Fallén) (Diptera, Anthomyiidae) on varieties of swedes and turnips. Norsk Entomologisk Tidsskrift 19:81–90.

    Google Scholar 

  • Scott, G. C. 1974. The response of wheat bulb fly larvae to cereal exudates and extracts. Ann. Appl. Biol. 77:107–111.

    Google Scholar 

  • Soni, S. K. and Finch, S. 1979. Laboratory evaluation of sulphur-bearing chemicals as attractants for larvae of the onion fly, Delia antiqua (Meigen) (Diptera: Anthomyiidae). Bull. Entomol. Res. 69:291–298.

    CAS  Google Scholar 

  • Staley, J. T. and Johnson, S. N. 2008. Climate change impacts on root herbivores, pp. 192–213, in S. N. Johnson and P. J. Murray (eds.), Root Feeders—An Ecosystem Perspective. CABI, Wallingford.

    Google Scholar 

  • Stokes, B. M. 1956. A chemotactic response in wheat bulb fly larvae. Nature 4537:801.

    Google Scholar 

  • Strnad, S. P. and Bergman, M. K. 1987a. Distribution and orientation of western corn-rootworm (Coleoptera, Chrysomelidae) larvae in corn roots. Environ. Entomol. 16:1193–1198.

    Google Scholar 

  • Strnad, S. P. and Bergman, M. K. 1987b. Movement of first instar Western corn rootworms (Coleoptera: Chrysomelidae) in soil. Environ. Entomol. 16:975–978.

    Google Scholar 

  • Strnad, S. P., Bergman, M. K., and Fulton, W. C. 1986. First instar western corn rootworm (Coleoptera, Chrysomelidae) response to carbon dioxide. Environ. Entomol. 15:839–842.

    Google Scholar 

  • Sutherland, O. R. W. 1972. Olfactory response of Costelytra zealandica (Coleoptera: Melolonthinae) larvae to grass root odours. N. Z. J. Sci. 15:165–172.

    Google Scholar 

  • Sutherland, O. R. W. and Hillier, J. R. 1974a. Feeding behaviour of the grass grub Costelytra zealandica (White) (Coleoptera: Melolonthinae) 3. The influence of amino acids, ascorbic acid, and inorganic salts. N. Z. J. Zool. 1:211–216.

    CAS  Google Scholar 

  • Sutherland, O. R. W. and Hillier, J. R. 1974b. Olfactory response of Costelytra zealandica (Coleoptera: Melolonthinae) to the roots of several pasture plants. N. Z. J. Zool. 1:365–369.

    Google Scholar 

  • Sutherland, O. R. W., Russell, G. B., and Biggs, D. R. 1980. Insect feeding deterrent activity of phytoalexin isoflavonoids. Biochem. Syst. Ecol. 8:73–75.

    CAS  Google Scholar 

  • Tapia, T., Perich, F., Pardo, F., Palma, G., and Quiroz, A. 2007. Identification of volatiles from differently aged red clover (Trifolium pratense) root extracts and behavioural responses of clover root borer (Hylastinus obscurus) (Marsham) (Coleoptera: Scolytidae) to them. Biochem. Syst. Ecol. 35:61–67.

    CAS  Google Scholar 

  • Thorpe, W. H., Crombie, A. C., Hill, R., and Darrah, J. H. 1946. The behaviour of wireworms in response to chemical stimulation. J. Exp. Biol. 23:234–266.

    Google Scholar 

  • van Dam, N. M. 2009. Belowground herbivory and plant defenses. Annu. Rev. Ecol. S. 40:373–391.

    Google Scholar 

  • van Gundy, S. D., Kirkpatrick, J. D., and Golden, J. 1977. Nature and role of metabolic leakage from root-knot nematode galls and infection by Rhizoctonia solani. J. Nematol. 9:113–121.

    PubMed  Google Scholar 

  • von Städler, E. 1971. The orientation and host plant selection of Psilae rosae F. (Diptera: Psilidae). Z. Angew. Entomol. 69:425–438.

    Google Scholar 

  • Weissteiner, S. and Schutz, S. 2006. Are different volatile pattern influencing host plant choice of belowground living insects? Mitt. Dtsch. Ges. Angew. Ent. 15:51–55.

    Google Scholar 

  • Wenke, K., Kai, M., and Piechulla, B. 2010. Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506.

    PubMed  CAS  Google Scholar 

  • Wolfson, J. L. 1987. Impact of rhizobium nodules on Sitona hispidulus, the clover root curculio. Entomol. Exp. Appl. 43:237–243.

    Google Scholar 

  • Wurst, S., Wagenaar, R., Biere, A., and van der Putten, W. H. 2010. Microorganisms and nematodes increase levels of secondary metabolites in roots and root exudates of Plantago lanceolata. Plant Soil 329:117–126.

    CAS  Google Scholar 

  • Xie, Y. S., Arnason, J. T., Philogene, B. J. R., Lambert, J. D. H., Atkinson, J., and Morand, P. 1990. Role of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) in the resistance of maize to western corn rootworm, Diabrotica virgifera virgifera (Leconte) (Coleoptera, Chrysomelidae). Can. Entomol. 122:1177–1186.

    CAS  Google Scholar 

  • Xie, Y. S., Arnason, J. T., Philogene, B. J. R., Atkinson, J., and Morand, P. 1992. Behavioral responses of western corn rootworm larvae to naturally-occurring and synthetic hydroxamic acids. J. Chem. Ecol. 18:945–957.

    CAS  Google Scholar 

  • Yeates, G. W., Saggar, S., Hedley, C. B., and Mercer, C. F. 1999. Increase in 14C-carbon translocation to the soil microbial biomass when five species of plant-parasitic nematodes infect roots of white clover. Nematology 1:295–300.

    Google Scholar 

  • Zhang, X., Johnson, S. N., Gregory, P. J., Crawford, J. W., Young, I. M., Murray, P. J., and Jarvis, S. C. 2006. Modelling the movement and survival of the root-feeding clover weevil, Sitona lepidus, in the root-zone of white clover. Ecol. Model. 190:133–146.

    Google Scholar 

  • Zhang, X., Johnson, S. N., Crawford, J. W., Gregory, P. J., and Young, I. M. 2007. A general random walk model for the leptokurtic distribution of organism movement: theory and application. Ecol. Model. 200:79–88.

    Google Scholar 

Download references

Acknowledgments

The authors are grateful for the invitation to write this article and to the two anonymous reviewers for their constructive comments and suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Scott N. Johnson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johnson, S.N., Nielsen, U.N. Foraging in the Dark – Chemically Mediated Host Plant Location by Belowground Insect Herbivores. J Chem Ecol 38, 604–614 (2012). https://doi.org/10.1007/s10886-012-0106-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0106-x

Keywords

Navigation