Hostname: page-component-7bb8b95d7b-wpx69 Total loading time: 0 Render date: 2024-09-25T12:13:12.722Z Has data issue: false hasContentIssue false
  • English
  • Français

How does a carabid predator find aggregations of slugs in the field? Electroantennograms and behavioural assays suggest chemical cues

Published online by Cambridge University Press:  09 March 2007

A.R. McKemey ,
D.M. Glen  and
W.O.C. Symondson
A.R. McKemey
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff, CF10 3TL, UK
D.M. Glen
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff, CF10 3TL, UK
W.O.C. Symondson*
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff, CF10 3TL, UK
*
*Fax: +44 (0) 29 20874305 E-mail: Symondson@Cardiff.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Field studies suggest that the generalist carabid predator and scavenger Pterostichus melanarius Illiger aggregates to patches with a higher density of slug prey. The mechanisms behind such aggregation are unknown. Experiments were conducted to test the hypothesis that they are responding to chemical cues. Electroantennograms (EAGs) showed no response by P. melanarius antennae to live, nematode-infected, injured or freshly killed slugs, but a strong response to dead slugs that had been allowed to decay for up to 48 h. Such a response would enable the beetles to find carrion in the field and may also, as dead prey are likely to be spatially correlated with live ones, provide a mechanism by which P. melanarius finds patches with a higher density of live slugs. Subsequent video analyses of P. melanarius responses to patches of slug mucus within arenas showed that beetles with intact antennae could detect these patches because they spent more time, and moved greater distances, within them and increased their rate of turning. Thus, at close range, P. melanarius used their antennae to detect slug mucus and hence, by implication, live slugs. The apparent contradiction between EAG data and behavioural experiments is discussed. Together these result confirm that P. melanariusdoes respond to chemical cues from its slug prey in ways that could lead to aggregation in areas of higher slug density in the field.

Type
Review Article
Information
Bulletin of Entomological Research , Volume 94 , Issue 3 , June 2004 , pp. 235 - 244
Copyright
Copyright © Cambridge University Press 2004

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

Ayre, K. (1995) Evaluation of carabid predators in arable land. PhD thesis, University of Newcastle upon Tyne, Newcastle.Google Scholar
Bell, W.J. (1990) Searching behavior patterns in insects. Annual Review of Entomology 35, 447–467.CrossRefGoogle Scholar
Bohan, D.A., Bohan, A.C., Glen, D.M., Symondson, W.O.C., Wiltshire, C.W. & Hughes, L. (2000) Spatial dynamics of predation by carabid beetles on slugs. Journal of Animal Ecology 69, 367–379.CrossRefGoogle Scholar
Bohan, D.A., Glen, D.M. & Symondson, W.O.C. (2001) Spatial dynamics of predation by carabid beetles: a response to Mair et al. (2001). Journal of Animal Ecology 70, 877–879.CrossRefGoogle Scholar
Borden, J.H. (1977) Behavioral response of Coleoptera to pheromones, allomones, and kairomones. pp. 169–198in Shorey, H.H. & McKelvey, J.J. (Eds) Chemical control of insect behavior: theory and application. New York, Wiley-Interscience.Google Scholar
Buckland, S.M. & Grime, J.P. (2000) The effects of trophic structure and soil fertility on the assembly of plant communities. Oikos 91, 336–352.CrossRefGoogle Scholar
Campobasso, C.P., Di Vella, G. & Introna, F. (2001) Factors affecting decomposition and Diptera colonization. Forensic Science International 120, 18–27.Google Scholar
Canjar, R., Yin, C.M., Stoffolando, J.G., Tomassini, Barbarossa I., Liscia, A. & Angioy, A.M. (1990) Influence of age on the electroantennogram response of the female blowfly (Phormia regina) (Diptera: Calliphoridae). Journal of Insect Physiology 36, 917–921.Google Scholar
Cook, A. (1989) Crowding effects on the growth of juvenile slugs (Limax pseudoflavus). pp. 193–200in Henderson, I.F. (Ed.) Slugs and snails in world agriculture. Thornton Heath, British Crop Protection Council.Google Scholar
Den Boer, P.J. (1982) Facts, hypotheses and models on the part played by food in the dynamics of carabid populations. pp. 81–96 in Feeding behaviour and accessibility of food for carabid beetles. Warsaw, Warsaw Agriculture University Press.Google Scholar
Den, Otter C.J. & Saini, R.K. (1985) Pheromone perception in the tsetse fly (Glossina morsitans morsitans). Entomologia Experimentalis et Applicata 39, 155–161.Google Scholar
Den Otter, C.J., Tchicaya, T. & Schutte, A.M. (1991) Effects of age, sex and hunger on the antennal olfactory sensitivity of tsetse flies. Physiological Entomology 16, 173–182.CrossRefGoogle Scholar
Digweed, S.C. (1994) Detection of mucus producing prey by Carabus nemoralis Müller and Scaphinotus marginatus Fischer (Coleoptera: Carabidae). Coleopterists Bulletin 48, 361–369.Google Scholar
Fry, J.C. (1993) Biological data analysis, a practical approach. Oxford, Oxford University Press.CrossRefGoogle Scholar
Hansen-Delkeskamp, E. (1992) Functional characterization of antennal contact chemoreceptors in the cockroach, Periplaneta americana. Journal of Insect Physiology 38, 813–822.CrossRefGoogle Scholar
Harwood, J.D., Sunderland, K.D. & Symondson, W.O.C. (2001) Living where the food is: web location by linyphiid spiders in relation to prey availability in winter wheat. Journal of Applied Ecology 38, 88–99.CrossRefGoogle Scholar
Harwood, J.D., Sunderland, K.D. & Symondson, W.O.C. (2003) Web-location by linyphiid spiders: prey-specific aggregation and foraging strategies. Journal of Animal Ecology 72, 745–756.CrossRefGoogle Scholar
Kellogg, F.E. (1970) Water vapour and carbon dioxide receptors in Aedes aegypti. Journal of Insect Physiology 16, 99–108.Google Scholar
Kennedy, J. (1978) The concepts of olfactory ‘arrestment’ and ‘attraction’. Physiological Entomology 3, 91–98.CrossRefGoogle Scholar
Kielty, J.P., Allen-Williams, L.J., Underwood, N. & Eastwood, E.A. (1996) Behavioral responses of three species of ground beetle (Coleoptera: Carabidae) to olfactory cues associated with prey and habitat. Journal of Insect Physiology 9, 237–250.Google Scholar
Kirkland, D. (1999) The use of semiochemicals to enhance the natural control of pests of arable crops by invertebrate predators. PhD thesis, Edinburgh University, Edinburgh.Google Scholar
Langan, A.M., Pilkington, G. & Wheater, C.P. (2001) Feeding preferences of a predatory beetle (Pterostichus madidus) for slugs exposed to lethal and non-lethal dosages of metaldehyde. Entomologia Experimentalis et Applicata 98, 245–248.CrossRefGoogle Scholar
Maddrell, S. (1969) Secretion by the malpighian tubules of Rhodnius. The movements of ions and water. Journal of Experimental Biology 51, 71–97.CrossRefGoogle Scholar
Mair, J. & Port, G. (2001) Predation by the carabid beetles Pterostichus madidus and Nebria brevicollis is affected by size and condition of the prey slug Deroceras reticulatum. Agriculture and Forest Entomology 3, 99–106.CrossRefGoogle Scholar
McKemey, A.R., Symondson, W.O.C., Glen, D.M. & Brain, P. (2001) Effect of slug size on predation by Pterostichus melanarius (Coleoptera: Carabidae). Biocontrol Science and Technology 11, 83–93.CrossRefGoogle Scholar
McKemey, A., Symondson, W.O.C. & Glen, D.M. (2003) Predation and prey size choice by the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae): the dangers of extrapolating from laboratory to field. Bulletin of Entomological Research 93, 227–234.CrossRefGoogle ScholarPubMed
Pakarinen, E. (1994) The importance of mucus as a defense against carabid beetles by the slug Arion fasciatus and Deroceras reticulatum. Journal of Molluscan Studies 60, 149–155.Google Scholar
Park, K.C. & Cork, A. (1999) Electrophysiological responses of antennal receptor neurons in female Australian sheep blowflies, Lucilia cuprina, to host odours. Journal of Insect Physiology 45, 85–91.Google Scholar
Riechert, S.E. & Harp, J.M. (1987) Nutritional ecology of spiders. pp. 645–672in Slansky, F. & Rodriguez, J.G. (Eds) Nutritional ecology of insects, mites, spiders and related invertebrates. New York, Wiley & Sons.Google Scholar
Schoonhoven, L.M. (1977) Insect chemosensory responses to plant and animal hosts. pp. 7–14 in Shorey, H.H. & McKelvey, J.J. (Eds) Chemical control of insect behavior: theory and application. New York, Wiley-Interscience.Google Scholar
Symondson, W.O.C. & Williams, I.B. (1997) Low-vacuum electron microscopy of carabid chemoreceptors: a new tool for the identification of live and valuable museum specimens. Entomologia Experimentalis et Applicata 85, 75–82.CrossRefGoogle Scholar
Symondson, W.O.C., Glen, D.M., Wiltshire, C.W., Langdon, C.J. & Liddell, J.E. (1996) Effects of cultivation techniques and straw disposal methods on predation by Pterostichus melanarius (Coleoptera: Carabidae) upon slugs (Gastropoda: Plumonata) in an arable field. Journal of Applied Ecology 33, 741–753.CrossRefGoogle Scholar
Symondson, W.O.C., Glen, D.M., Ives, A.R., Langdon, C.J. & Wiltshire, C.W. (2002a) Dynamics of the relationship between a generalist predator and slugs over five years. Ecology 83, 137–147.CrossRefGoogle Scholar
Symondson, W.O.C., Sunderland, K.D. & Greenstone, M.H. (2002b) Can generalist predators be effective biocontrol agents? Annual Review of Entomology 47, 561–594.Google Scholar
Van Alphen, J.J.M. & Jervis, M.A. (1996) Foraging behaviour. pp. 1–62in Jervis, M.A. & Kidd, N. (Eds) Insect natural enemies. London, Chapman & Hall.Google Scholar
Vet, L.E.M., De Jong, R., Van Giessen, W. & Visser, J.H. (1990) A learning-related variation in electroantennogram responses of a parasitic wasp. Physiological Entomology 15, 243–247.CrossRefGoogle Scholar
Wallin, H. & Ekbom, B.S. (1994) Influence of hunger level and prey densities on movement patterns in three species of Pterostichus beetles (Coleoptera: Carabidae). Environmental Entomology 23, 1171–1181.CrossRefGoogle Scholar
Wheater, C.P. (1989) Prey detection by some predatory Coleoptera (Carabidae and Staphylinidae). Journal of Zoology 218, 171–185.CrossRefGoogle Scholar
Wheater, C.P. (1991) Effect of starvation on locomotor activity in some predacious Coleoptera (Carabidae, Staphylinidae). Coleopterists Bulletin 45, 371–378.Google Scholar
White, R.A., Paim, U. & Seabrook, W.D. (1974) Maxillary and labial sites of carbon dioxide-sensitive receptors of larval Orthosoma brunneum (Forster) (Coleoptera, Cerambycidae). Journal of Comparative Physiology 88, 235–246.CrossRefGoogle Scholar
Winder, L., Alexander, C.J., Holland, J.M., Woolley, C. & Perry, J.N. (2001) Modeling the dynamic spatio-temporal response of predators to transient prey patches in the field. Ecology Letters 4, 568–576.CrossRefGoogle Scholar