Hostname: page-component-76dd75c94c-sgvz2 Total loading time: 0 Render date: 2024-04-30T07:33:36.553Z Has data issue: false hasContentIssue false

Behavioural response of wheat bulb fly (Delia coarctata, Diptera: Anthomyiidae) larvae to the primary plant metabolite carbon dioxide

Published online by Cambridge University Press:  10 July 2013

C.D. Rogers*
Affiliation:
Institute of Evolutionary Biology, University of Edinburgh Ashworth Laboratories, Edinburgh EH9 3JT, UK SRUC, West Mains Road, Edinburgh EH9 3JG, UK
K.A. Evans
Affiliation:
SRUC, West Mains Road, Edinburgh EH9 3JG, UK
J. Parker
Affiliation:
SRUC, West Mains Road, Edinburgh EH9 3JG, UK
V.A. Pappa
Affiliation:
Züricher Hochschule für Angewandte Wissenschaften, Institut Umwelt und Natürliche Ressourcen, Grüental 8820, Wädenswil, Switzerland
*
*Author for correspondence Fax: +44 (0)131 535 4144 Phone: +44 (0)7725649393 E-mail: craigrogers22@hotmail.com

Abstract

Wheat bulb fly (WBF) larvae use chemotaxis to orientate towards host-plant root exudates. This study aimed to investigate the role of the primary plant metabolite carbon dioxide (CO2) in host-plant location by WBF. Arena based behavioural experiments were used to identify whether CO2 induced chemotaxis (directional movement in response to a chemical stimulus) or kinesis (non-directional movement in response to a stimulus) from WBF larvae. No chemotactic response was observed when larvae were presented to a point source of CO2. However, elevated levels of CO2 induced kinesis, with both track length and tortuosity (number of twists and turns in the movement path) increasing at elevated CO2 levels of 1000–2000 ppm, demonstrating increased searching behaviour. Soil emission of CO2 was quantified to compare soil levels with those identified as eliciting behavioural effects on the larvae. Samples removed from soil gave a mean CO2 concentration of 557 (±46) ppm, which is lower than the lowest concentration of CO2 found to induce a behavioural response and higher than the lowest CO2 concentration tested, which was found not to alter behaviour. It is proposed that increased CO2 concentrations in the soil act as a behavioural trigger, inducing intensive searching of an area by WBF larvae. This increases the likelihood of finding more host-specific identifiers, such as secondary metabolites when near a potential host-plant.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adler, J. (1966) Chemotaxis in bacteria. Science 153, 708716.CrossRefGoogle ScholarPubMed
Barrozo, R.B. & Lazzari, C.R. (2004) The response of the blood-sucking bug Triatoma infestans to carbon dioxide and other host odours. Chemical Senses 29, 319329.Google Scholar
Bellows, T.S. & Fisher, T.W. (1999) Handbook of Biological Control: Principles and Applications. San Diego, Academic Press.Google Scholar
Bernklau, E.J. & Bjostad, L.B. (1998) Reinvestigation of host location by western corn rootworm larvae (Coleoptera: Chrysomelidae): CO2 is the only volatile attractant. Journal of Economic Entomology 91, 13311340.Google Scholar
Bernklau, E.J., Fromm, E.A. & Bjostad, L.B. (2004) Disruption of host location of western corn rootworm larvae (Coleoptera: Chrysomelidae) with carbon dioxide. Journal of Economic Entomology 97, 330339.Google Scholar
Bhasin, A., Mordue, A.J. & Mordue, W. (2001) Field studies on efficacy of host odour baits for the biting midge Culicoides impunctatus in Scotland. Medical and Veterinary Entomology 15, 147156.Google Scholar
Bjostad, L.B. & Hibbard, B.E. (1992) 6-methoxy-2-benzoxazolinone a semiochemical for host location by western corn rootworm larvae. Journal of Chemical Ecology 18, 931944.Google Scholar
Cardé, R.T. & Minks, A.K. (1995) Control of moth pests by mating disruption: success and constraints. Annual Review of Entomology 40, 559585.CrossRefGoogle Scholar
DeFoliart, G.R. & Morris, G.D. (1967) A dry ice-baited trap for the collection and field storage of hematophagous Diptera. Journal of Medical Entomology 4, 360363.Google Scholar
Doerr, V.J. & Doerr, E.D. (2004) Fractal analysis can explain individual variation in dispersal search paths. Ecology 85, 14281438.CrossRefGoogle Scholar
Eisenbach, M. (2004) Chemotaxis. London, Imperial College Press.Google Scholar
Fowler, J., Cohen, L. & Jarvis, P. (1998) Practical Statistics for Field Biology. Chichester, John Wiley & Sons Ltd.Google Scholar
Galbreath, R.A. (1988) Orientation of grass grub Costelytra zealandica (Coleoptera: Scarabaeidae) to a carbon dioxide source. New Zealand Entomologist 11, 67.Google Scholar
Gillott, C. (2005) Entomology, 3rd edn. Dordrecht, Springer.Google Scholar
Gollany, H.T., Schumacher, T.E., Rue, R.R. & Liu, S.Y. (1993) A carbon dioxide microelectrode for in situ CO2 measurement. Microchemical Journal 48, 4249.Google Scholar
Greenway, A.R., Scott, G.C., Calam, D.H. & Smith, M.C. (1976) Chemistry of components in wheat and oats that influence behaviour of wheat bulb fly larvae. Journal of Insect Physiology 22, 445451.CrossRefGoogle Scholar
Hanson, P.J., Edwards, N.T., Garten, C.T. & Andrews, J.A. (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48, 115146.Google Scholar
Hayakawa, H. (1988) Relationship between the volume of carbon dioxide and the effectiveness in collecting tabanid flies. Japanese Journal of Sanitary Zoology 39, 313315.Google Scholar
Hiltpold, I. & Turlings, T.C.J. (2012) Manipulation of chemically mediated interactions in agricultural soils to enhance the control of crop pests and to improve crop yield. Journal of Chemical Ecology 38, 641650.Google Scholar
Honda, I. & Ishikawa, Y. (1987) Electrophysiological studies on the dorsal and anterior organs of the onion fly larva, Hylemya antiqua Meigen (Diptera, Anthomyiidae). Applied Entomology and Zoology 22, 410416.CrossRefGoogle Scholar
Hopkins, R.J., Griffiths, D.W., Birch, A.N.E., McKinlay, R.G. & Hall, J.E. (1993) Relationships between turnip root fly (Delia floralis) larval development and the sugar content of swede (Brassica napus ssp. rapifera) roots. Annals of Applied Biology 122(3), 405415.Google Scholar
Huang, X.P. & Mack, T.P. (2001) Artificial carbon dioxide source to attract lesser cornstalk borer (Lepidoptera: Pyralidae) larvae. Journal of Economic Entomology 94(4), 860867.Google Scholar
Jewett, D.K. & Bjostad, L.B. (1996) Dichloromethane attracts diabroticite larvae in a laboratory behavioral bioassay. Journal of Chemical Ecology 22(7), 13311344.Google Scholar
Johnson, S.N. & Gregory, P.J. (2006) Chemically-mediated host-plant location and selection by root-feeding insects. Physiological Entomology 31(1), 113.CrossRefGoogle Scholar
Johnson, S.N. & Nielsen, U.N. (2012) Foraging in the dark – chemically mediated host plant location by belowground insect herbivores. Journal of Chemical Ecology 38(6), 604614.CrossRefGoogle ScholarPubMed
Johnson, S.N., Zhang, X.X., Crawford, J.W., Gregory, P.J., Hix, N.J., Jarvis, S.C., Murray, P.J. & Young, I.M. (2006) Effects of carbon dioxide on the searching behaviour of the root-feeding clover weevil Sitona lepidus (Coleoptera: Curculionidae). Bulletin of Entomological Research 96(4), 361366.Google Scholar
Jones, O.T. & Coaker, T.H. (1977) Oriented responses of carrot fly larvae, Psila rosae, to plant odours, carbon dioxide and carrot root volatiles. Physiological Entomology 2(3), 189197.Google Scholar
Jones, O.T. & Coaker, T.H. (1978) A basis for host plant finding in phytophagous larvae. Entomologia Experimentalis et Applicata 24, 272284.Google Scholar
Klingler, J. (1957) Über die bedeutung des kohlendioxyds für die orientierung der larven von Otiorrhynchus sulcatus F., Melolontha und Agriotes (Col.) im boden (Vorlaufige mitteilung). Mitteilungen der Schweizerischen Entomologischen Gesellschaft 30, 317322.Google Scholar
Levine, E. & Oloumi-Sadeghi, H. (1991) Management of diabroticite rootworms in corn. Annual Review of Entomology 36, 229255.Google Scholar
Mandelbrot, B. (1967) How long is the coast of Britain? Statistical self-similarity and fractional dimension. Science 156, 636638.Google Scholar
Mandelbrot, B.B. (1983) The Fractal Geometry of Nature. New York, W.H. Freeman and Co.Google Scholar
Marriott, C. (2001) Host plant location, selection and preference by wheat bulb fly Delia coarctata Fall. (Diptera: Anthomyiidae). PhD Thesis, University of Edinburgh.Google Scholar
Marriott, C. & Evans, K.A. (2003) Host plant choice and location by larvae of the wheat bulb fly (Delia coarctata). Entomologia Experimentalis et Applicata 106(1), 16.Google Scholar
Milne, B.T. (1991) Lessons from applying fractal models to landscape patterns. pp. 199235in Turner, M.G. & Gardner, R.H. (Eds) Quantitative Methods in Landscape Ecology. New York, Springer.CrossRefGoogle Scholar
Milne, B.T. (1997) Applications of fractal geometry in wildlife biology. pp. 3269in Bissonette, J.A. (Ed.) Wildlife and Landscape Ecology. New York, Springer-Verlag.Google Scholar
Morris, H.M. (1925) Note on the wheat bulb fly (Leptohylemyia coarctata, Fall.). Bulletin of Entomological Research 15, 359360.CrossRefGoogle Scholar
Nams, V.O. (1996) The VFractal: a new estimator for fractal dimension of animal movement paths. Landscape Ecology 11(5), 289297.Google Scholar
Nams, V.O. (2005) Using animal movement paths to measure response to spatial scale. Oecologia 143, 179188.Google Scholar
Nansen, C., MacDonald, K.M., Rogers, C.D., Thomas, M., Poppy, G.M. & Baxter, I.H. (2007) Effects of sex pheromone in electrostatic powder on mating behaviour by Lobesia botrana males. Journal of Applied Entomology 131(5), 303310.Google Scholar
Nelson, R.L. (1965) Carbon dioxide as an attractant for Culicoides. Journal of Medical Entomology 2(1), 5657.Google Scholar
Payne, D. & Gregory, P.J. (1988) The soil atmosphere. pp. 298314in Wild, A. (Ed.) Russell's Soil Conditions and Plant Growth. Harlow, Longman.Google Scholar
Petherbridge, F.R. (1921) Observations on the life history of the wheat-bulb fly Leptohylenyia coarctata, Fall. Journal of Agricultural Science 11, 99105.Google Scholar
Rogers, C.D. (2011) Ecological and molecular investigation of wheat bulb fly (Delia coarctata, Fallén, Diptera: Anthomyiidae) for the advancement of population monitoring and control methodologies. PhD Thesis, University of Edinburgh.Google Scholar
Rogers, C.D. & Evans, K.A. (2013) Wheat bulb fly (Delia coarctata, Fallén, Diptera: Anthomyiidae) larval response to hydroxamic acid constituents of host-plant root exudates. Bulletin of Entomological Research 103(3), 261268.Google Scholar
Scott, G.C. (1974) The response of wheat bulb fly larvae to cereal exudates and extracts. Annals of Applied Biology 77(1), 107111.Google Scholar
Sheppard, S.K. & Lloyd, D. (2002) Direct mass spectrometric measurement of gases in soil monoliths. Journal of Microbiological Methods 50, 175188.Google Scholar
Stokes, B.M. (1956) A chemotactic response in wheat bulb fly larvae. Nature 178, 801.Google Scholar
Strnad, S.P., Bergman, M.K. & Fulton, W.C. (1986) First instar western corn rootworm (Coleoptera, Chrysomelidae) response to carbon dioxide. Environmental Entomology 15(4), 839842.Google Scholar
Taiz, L. & Zeiger, E. (2010) Plant Physiology. Sunderland, Sinauer Associates Inc.Google Scholar
Tepe, J.B. & Dodge, B.F. (1943) Absorption of carbon dioxide by sodium hydroxide solutions in a packed column. Transactions of the American Institute of Chemical Engineers 39, 255.Google Scholar
Thorpe, W.H., Crombie, A.C., Hill, R. & Darrah, J.H. (1947) The behaviour of wireworms in response to chemical stimulation. Journal of Experimental Biology 23(3–4), 234266.CrossRefGoogle ScholarPubMed
Turlings, T.C.J., Hiltpold, I. & Rasmann, S. (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358(1), 5160.Google Scholar
Turner, S.L., Li, N., Guda, T., Githure, J., Cardé, R.T. & Ray, A. (2011) Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes. Nature 474, 8791.Google Scholar
Way, M.J. (1959) The effect of temperature, particularly during diapause, on the development of the egg of Leptohylemyia coarctata Fallen (Diptera: Muscidae). Transactions of the Royal Entomological Society of London 111(12), 351364.CrossRefGoogle Scholar
Wiens, J.A., Crist, T.O., With, K.A. & Milne, B.T. (1995) Fractal patterns of insect movement in microlandscape mosaics. Ecology 76, 663666.Google Scholar
Williams, C.R., Long, S.A., Russell, R.C. & Ritchie, S.A. (2006) Field efficacy of the BG-Sentinel compared with CDC Backpack Aspirators and CO2-baited EVS traps for collection of adult Aedes aegypti in Cairns, Queensland, Australia. Journal of the American Mosquito Control Association 22(2), 296–230.Google Scholar