Skip to main content Accessibility help
×
Home

Predation by beetles (Carabidae, Staphylinidae) on eggs and juveniles of the Iberian slug Arion lusitanicus in the laboratory

  • B.A. Hatteland (a1), K. Grutle (a2), C.E. Mong (a1), J. Skartveit (a3), W.O.C. Symondson (a4) and T. Solhøy (a1)...

Abstract

Arion lusitanicus has become a major pest species in western Norway in the last few years. This species originates from southern Europe but has been spread by humans over large parts of central and northern Europe during recent decades. Slugs have traditionally been controlled by the use of molluscicides; but, as these may have serious ecological side effects, biological control of slugs is highly desirable. Potential biological control agents include nematodes, gastropods and arthropods. In laboratory experiments, we tested whether five common predator beetles would feed on eggs and juveniles of A. lusitanicus. The species Carabus nemoralis, Nebria brevicollis, Pterostichus melanarius and Pterostichus niger (Carabidae) as well as Staphylinus erythropterus (Staphylinidae) were tested, of which only P. melanarius has been tested on A. lusitanicus previously. Nebria brevicollis did not feed on slug eggs or newly hatched slugs, but the remaining four species all killed and ate a large proportion of the eggs and hatchlings offered. Both P. melanarius and P. niger also destroyed A. lusitanicus eggs and hatchlings under conditions emulating those in the field. Prey size choice experiments were conducted by feeding C. nemoralis, P. niger and S. erythropterus on different sizes of A. lusitanicus. Carabus nemoralis was also given a choice between two slug species, A. lusitanicus and Deroceras reticulatum. A significant preference for slugs smaller than one gram was evident for C. nemoralis, while the other beetles struggled much more to overcome the mucus of juvenile slugs. No significant preference was found between A. lusitanicus and D. reticulatum as prey for C. nemoralis. We also discuss the feasibility of biological control of A. lusitanicus using beetle predators.

Copyright

Corresponding author

*Author for correspondence Fax: +47 55 58 44 50 E-mail: Bjorn.hatteland@bio.uib.no

References

Hide All
Altieri, M.A., Hagen, K.S., Trujillo, J. & Caltagirone, L.E. (1982) Biological control of Limax maximus and Helix aspersa by indigenous predators in a daisy field in central coastal California. Acta Oecologia 3, 387390.
Anderson, R. (2005) An annotated list of the non-marine Mollusca of Britain and Ireland. Journal of Conchology 38, 607.
Asteraki, E.J. (1993) The potential of carabid beetles to control slugs in grass/clover swards. Entomophaga 38, 193198.
Ayre, K. (2001) Effect of predator size and temperature on the predation of Deroceras reticulatum (Müller) (Mollusca) by carabid beetles. Journal of Applied Entomology 125, 389395.
Barker, G.M. (2002) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.
Bless, R. (1977) Studies on the relationships of carabids as predators to gastropods as prey. Anzeiger für Schadlingskunde, Pflanzenschutz, Umweltschutz 50, 5557.
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, 367379.
Dodd, C.S. (2004) Development and optimisation of PCR-based techniques in predator gut analysis. PhD thesis, Cardiff University, Cardiff, UK.
Dolmen, D. & Winge, K. (1997) Boasneglen (Limax maximus) og iberiasneglen (Arion lusitanicus) i Norge; utbredelse, spredning og skadevirkninger (In Norwegian). ‘Limax maximus and Arion lusitanicus in Norway: distribution, expansion and injurious effects’, Report 4, 4–24. Trondheim, Norway, Vitenskapsmuseet.
Eilenberg, J., Hajek, A. & Lomer, C. (2001) Suggestions for unifying the terminology in biological control. BioControl 46, 387400.
Essl, F. & Rabitsch, W. (2002) Neobiota in Österreich. Vienna, Austria, Umweltbundesamt.
Glück, E. & Kreisel, A. (1986) Die Hecke als Lebensraum, Refugium und Vernetzungsstruktur und ihre Bedeutung für die Dispersion von Waldcarabidenarten. Laufener Seminarbeiträge 10, 6483.
Grimm, B., Paill, W. & Kaiser, H. (2000) Daily activities of the pest slug Arion lusitanicus. Journal of Molluscan Studies 66, 125130.
Gruttke, H. (1994) Dispersal of carabid species along a linear sequence of young hedge plantations. pp. 299303in Desender, K., Dufrêne, M., Loreau, M., Luff, M.L. & Maelfait, J.-P. (Eds) Carabid Beetles: Ecology and Evolution. Kluwer Academic Publishers.
Harper, G.L., King, R.A., Dodd, C.S., Harwood, J.D., Glen, D.M., Bruford, M.W. & Symondson, W.O.C. (2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Molecular Ecology 14, 819827.
Hengeveld, R. (1980a) Food specialization in ground beetles: an ecological or a phylogenetic process? (Coleoptera, Carabidae). Netherlands Journal of Zoology 30, 585594.
Hengeveld, R. (1980b) Qualitative and quantitative aspects of the food of ground beetles (Coleoptera, Carabidae): a review. Netherlands Journal of Zoology, 30, 555563.
Hommay, G. (2002) Agriolimacidae, Arionidae and Milacidae as pests in West European sunflower and maize. pp. 245254in Barker, G.M. (Ed.) Molluscs as crop pests. CABI Publishing, Wallingford, UK.
Iglesias, J., Castillejo, J., Ester, A., Castro, R. & Lombardia, M.J. (2002) Susceptibility of the eggs of the field slug Deroceras reticulatum to contact with pesticides and substances of biological origin on artificial soil. Annales of Applied Biology 140, 5359.
Kaiser, H., Geiersberger, U., Grimm, B. & Paill, W. (1993) Untersuchungen über die biologischen und ökologischen Voraussetzungen des Massenauftretens der Spanischen Wegschnecke. Final report. Graz, Austria.
Keller, M., Kollmann, J. & Edwards, P.J. (1999) Palatibility of weeds from different European origins to the slugs Deroceras reticulatum Müller and Arion lusitanicus Mabille. Acta Oecologica 20, 109118.
Langan, A.M., Taylor, A. & Wheater, C.P. (2004) Effects of metaldehyde and methiocarb on feeding preferences and survival of a slug predator (Pterostichus melanarius (F.): Carabidae, Pterostichini). Journal of Applied Entomology 128, 5155.
Lindroth, C.H. (1985) The Carabidae (Coleoptera) of Fennoscandia and Denmark. Vol. 1. Fauna Entomologica Scandinavica 15, 1225.
Lindroth, C.H. (1986) The Carabidae (Coleoptera) of Fennoscandia and Denmark. Vol. 2. Fauna Entomologica Scandinavica 15, 226497.
Luff, M.L. (2007) The Carabidae (ground beetles) of Britain and Ireland, 2nd edn.Royal Entomological Society, St Albans, UK.
Mair, J. & Port, G.R. (2001) Predation on the slug Deroceras reticulatum by the carabid beetles Pterostichus madidus and Nebria brevicollis in the presence of alternative prey. Agriculture and Forest Entomology 3, 169174.
McKemey, A.R., Symondson, W.O.C., Glen, D.M. & Brain, P. (2001) Effects of slug size on predation by Pterostichus melanarius (Coleoptera: Carabidae). Biocontrol Science and Technology 11, 8191.
McKemey, A.R., 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, 227234.
Mendis, V.W., Bowen, I.D., Liddell, J.E. & Symondson, W.O.C. (1996) Monoclonal antibodies against Deroceras reticulatum and Arion ater eggs for use in predation studies. pp. 99–106 in Henderson, I. (Ed.) Slug and snail pests in agriculture. BCPC Symposium Proceedings No. 66. Farnham, UK: British Crop Protection Council.
Oberholzer, F. & Frank, T. (2003) Predation by the carabid beetles Pterostichus melanarius and Poecilus cupreus on slugs and slug eggs. Biocontrol Science and Technology 13, 99–110.
Oberholzer, F., Escher, N. & Frank, T. (2003) The potential of carabid beetles (Coleoptera) to reduce slug damage to oilseed rape in the laboratory. European Journal of Entomology 100, 8185.
Paill, W. (2000) Slugs as prey for larvae and imagines of Carabus violaceus L. (Coleoptera, Carabidae). pp. 221–22 in Brandmayr, P., Lövei, G.L., Brandmayr, T.Z., Casale, A. & Vigna Taglianti, A. (Eds) Natural history and applied ecology of carabid beetles. Sofia, Bulgaria, Pensoft Publishers.
Paill, W. (2004) Slug feeding in the carabid beetle Pterostichus melanarius: seasonality and dependence on prey size. Journal of Molluscan Studies 70, 203205.
Pakarinen, E. (1994) The importance of mucus as a defence against carabid beetles by the slugs Arion fasciatus and Deroceras reticulatum. Journal of Molluscan Studies 60, 149155.
Port, C.M. & Port, G. (1986) The biology and behaviour of slugs in relation to crop damage and control. Agricultural Zoology Reviews 1, 255299.
Poulin, G. & O'Neil, L.G. (1969) Observations sur les prédators de la limace noire, Arion ater (L.) (Gastéropodes, Pulmonés, Arionidés). Phytoprotection 50, 16.
R Development Core Team, (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Available online at http://www.R-project.org.
Schroeder, F.C., Gonzalez, A., Eisner, T. & Meinwald, J. (1999) Miriamin, a defence diterpene from the eggs of a land slug (Arion sp.). Proceedings of the National Academy of Sciences USA 96, 1362013625.
South, A. (1992) Terrestrial Slugs: Biology, Ecology and Ccontrol. London, UK, Chapman & Hall.
Sunderland, K.D. (2002) Invertebrate pest control of slugs by carabids. pp. 165214in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.
Symondson, W.O.C. (1993) The effects of crop development upon slug distribution and control by Abax parallelepipedus (Coleoptera, Carabidae). Annales of Applied Biology 123, 449457.
Symondson, W.O.C. (1994) The potential of Abax parallelepipedus (Coleoptera, Carabidae) for mass breeding as a biological control agent against slugs. Entomophaga 39, 323333.
Symondson, W.O.C. (2002) Diagnostic techniques for determining carabid diets. pp. 111164in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.
Symondson, W.O.C. (2004) Coleoptera (Carabidae, Staphylinidae, Lampyridae, Drilidae and Silphidae) as predators of terrestrial gastropods. pp. 3784in Barker, G.M. (Ed.) Natural Enemies of Terrestrial Molluscs. Oxford, UK, CAB International.
Symondson, W.O.C., Mendis, V.W. & Liddell, J.E. (1995) Monoclonal antibodies for the identification of slugs and their eggs. EPPO Bulletin 25, 377382.
Symondson, W.O.C., Glen, D.M., Whiltshire, C.W., Langdon, C.J. & Liddell, J.E. (1996) Effects of cultivation techniques and methods of straw disposal on predation by Pterostichus melanarius (Coleoptera: Carabidae) upon slugs (Gastropoda: Pulmonata) in an arable field. Journal of Applied Ecology 33, 741753.
Symondson, W.O.C., Glen, D.M., Ives, A.R., Langdon, C.J. & Wiltshire, C.W. (2002) Dynamics of the relationship between a generalist predator and slugs over five years. Ecology 83, 137147.
Thiele, H.U. (1977) Carabid Beetles in their Environments. Berlin, Germany, Springer Verlag.
Thomas, R.S. (2002) An immunological and behavioural study of the role of carabid beetle larvae as slug control agents in cereal crops. PhD thesis, Cardiff University, Cardiff, UK.
Thomas, R.S., Glen, D.M. & Symondson, W.O.C. (2008) Prey detection through olfaction by the soil-dwelling larvae of the carabid predator Pterostichus melanarius. Soil Biology and Biochemistry 40, 207216.
Thomas, R.S., Harwood, J.D., Glen, D.M. & Symondson, W.O.C. (2009) Molecular tracking of subterranean density-dependent predation by carabid larvae on slugs. Ecological Entomology 34, 569579.
Tod, M.E. (1973) Notes on beetle predators of mollusks. The Entomologist 106, 196201.
Toft, S. & Bilde, T. (2002) Carabid diets and food value. pp. 81–110 in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.
Tomasgård, T.E.H. (2005) Populasjonsdynamikk, næringspreferansar og reproduksjon/vekst hjå snilen Arion lusitanicus Mabille, 1868 (In Norwegian). ‘Population dynamics, food preferences, reproduction and growth in the slug Arion lusitanicus Mabille, 1868’. Unpublished Candidata Scientiarum-thesis, University of Bergen, Bergen, Norway.
Traugott, M. (1998) Larval and adult species composition, phenology and life cycles of carabid beetles (Coleoptera, Carabidae) in an organic potato field. European Journal of Soil Biology 34, 189197.
Turin, H., Penev, L., Casale, A., Arndt, E., Assman, T., Makarov, K., Mossakowski, D., Szél, G. & Weber, F. (2003) Species accounts. pp. 151284in Turin, H., Penev, L. & Casale, A. (Eds) The Genus Carabus in Europe: A Synthesis. Sofia, Bulgaria, Pensoft Publishers.
von Proschwitz, T. (1996) Utbredning och spredning av spansk skogssnigel (Arion lusitanicus Mabille) och röd skogssnigel (Arion rufus L.) – en oversikt av utveclingen i Sverige (In Swedish). ‘Distribution and spreading of the Iberian slug (Arion lusitanicus Mabille) and the red slug (Arion rufus L.) – an overview of the development in Sweden’. Göteborgs Naturhistoriska Museums årstryck 1996, 2739.
von Proschwitz, T. & Winge, K. (1994) Iberiaskogsnegl – en art på spredning i Norge (In Norwegian). ‘The Iberian slug – a species expanding in Norway’. Fauna 47, 195203.
Zar, J.H. (1999) Biostatical Analysis, 4th edn. New Jersey, USA, Prentice-Hall.

Keywords

Predation by beetles (Carabidae, Staphylinidae) on eggs and juveniles of the Iberian slug Arion lusitanicus in the laboratory

  • B.A. Hatteland (a1), K. Grutle (a2), C.E. Mong (a1), J. Skartveit (a3), W.O.C. Symondson (a4) and T. Solhøy (a1)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed