Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-15T17:16:09.717Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  17 February 2010

B.A. Hatteland ,
K. Grutle ,
C.E. Mong ,
J. Skartveit ,
W.O.C. Symondson  and
T. Solhøy
B.A. Hatteland*
Affiliation:
Department of Biology, University of Bergen, Post Box 7803, N-5020Bergen, Norway
K. Grutle
Affiliation:
Student Services, College of Stord/Haugesund, Post Box 5000, N-5409Stord, Norway
C.E. Mong
Affiliation:
Department of Biology, University of Bergen, Post Box 7803, N-5020Bergen, Norway
J. Skartveit
Affiliation:
NLA Teacher Training College, Olav Bjordalsvei 41, 5111Breistein, Norway
W.O.C. Symondson
Affiliation:
School of Biosciences, University of Cardiff, PO Box 915, CardiffCF10 3TL, UK
T. Solhøy
Affiliation:
Department of Biology, University of Bergen, Post Box 7803, N-5020Bergen, Norway
*
*Author for correspondence Fax: +47 55 58 44 50 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

ArionDerocerasbiological controlCarabidaeinvasive speciespredationStaphylinidae
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 100 , Issue 5 , October 2010 , pp. 559 - 567
Copyright
Copyright © Cambridge University Press 2010

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

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, 387–390.Google Scholar
Anderson, R. (2005) An annotated list of the non-marine Mollusca of Britain and Ireland. Journal of Conchology 38, 607.Google Scholar
Asteraki, E.J. (1993) The potential of carabid beetles to control slugs in grass/clover swards. Entomophaga 38, 193–198.CrossRefGoogle Scholar
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, 389–395.CrossRefGoogle Scholar
Barker, G.M. (2002) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Bless, R. (1977) Studies on the relationships of carabids as predators to gastropods as prey. Anzeiger für Schadlingskunde, Pflanzenschutz, Umweltschutz 50, 55–57.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
Dodd, C.S. (2004) Development and optimisation of PCR-based techniques in predator gut analysis. PhD thesis, Cardiff University, Cardiff, UK.Google Scholar
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.Google Scholar
Eilenberg, J., Hajek, A. & Lomer, C. (2001) Suggestions for unifying the terminology in biological control. BioControl 46, 387–400.CrossRefGoogle Scholar
Essl, F. & Rabitsch, W. (2002) Neobiota in Österreich. Vienna, Austria, Umweltbundesamt.Google Scholar
Glück, E. & Kreisel, A. (1986) Die Hecke als Lebensraum, Refugium und Vernetzungsstruktur und ihre Bedeutung für die Dispersion von Waldcarabidenarten. Laufener Seminarbeiträge 10, 64–83.Google Scholar
Grimm, B., Paill, W. & Kaiser, H. (2000) Daily activities of the pest slug Arion lusitanicus. Journal of Molluscan Studies 66, 125–130.CrossRefGoogle Scholar
Gruttke, H. (1994) Dispersal of carabid species along a linear sequence of young hedge plantations. pp. 299–303in Desender, K., Dufrêne, M., Loreau, M., Luff, M.L. & Maelfait, J.-P. (Eds) Carabid Beetles: Ecology and Evolution. Kluwer Academic Publishers.CrossRefGoogle Scholar
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, 819–827.CrossRefGoogle ScholarPubMed
Hengeveld, R. (1980a) Food specialization in ground beetles: an ecological or a phylogenetic process? (Coleoptera, Carabidae). Netherlands Journal of Zoology 30, 585–594.CrossRefGoogle Scholar
Hengeveld, R. (1980b) Qualitative and quantitative aspects of the food of ground beetles (Coleoptera, Carabidae): a review. Netherlands Journal of Zoology, 30, 555–563.CrossRefGoogle Scholar
Hommay, G. (2002) Agriolimacidae, Arionidae and Milacidae as pests in West European sunflower and maize. pp. 245–254in Barker, G.M. (Ed.) Molluscs as crop pests. CABI Publishing, Wallingford, UK.CrossRefGoogle Scholar
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, 53–59.CrossRefGoogle Scholar
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.Google Scholar
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, 109–118.CrossRefGoogle Scholar
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, 51–55.CrossRefGoogle Scholar
Lindroth, C.H. (1985) The Carabidae (Coleoptera) of Fennoscandia and Denmark. Vol. 1. Fauna Entomologica Scandinavica 15, 1–225.Google Scholar
Lindroth, C.H. (1986) The Carabidae (Coleoptera) of Fennoscandia and Denmark. Vol. 2. Fauna Entomologica Scandinavica 15, 226–497.Google Scholar
Luff, M.L. (2007) The Carabidae (ground beetles) of Britain and Ireland, 2nd edn.Royal Entomological Society, St Albans, UK.Google Scholar
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, 169–174.CrossRefGoogle Scholar
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, 81–91.CrossRefGoogle Scholar
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, 227–234.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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, 81–85.CrossRefGoogle Scholar
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.Google Scholar
Paill, W. (2004) Slug feeding in the carabid beetle Pterostichus melanarius: seasonality and dependence on prey size. Journal of Molluscan Studies 70, 203–205.CrossRefGoogle Scholar
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, 149–155.CrossRefGoogle Scholar
Port, C.M. & Port, G. (1986) The biology and behaviour of slugs in relation to crop damage and control. Agricultural Zoology Reviews 1, 255–299.Google Scholar
Poulin, G. & O'Neil, L.G. (1969) Observations sur les prédators de la limace noire, Arion ater (L.) (Gastéropodes, Pulmonés, Arionidés). Phytoprotection 50, 1–6.Google Scholar
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.Google Scholar
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, 13620–13625.CrossRefGoogle ScholarPubMed
South, A. (1992) Terrestrial Slugs: Biology, Ecology and Ccontrol. London, UK, Chapman & Hall.CrossRefGoogle Scholar
Sunderland, K.D. (2002) Invertebrate pest control of slugs by carabids. pp. 165–214in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.Google Scholar
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, 449–457.CrossRefGoogle Scholar
Symondson, W.O.C. (1994) The potential of Abax parallelepipedus (Coleoptera, Carabidae) for mass breeding as a biological control agent against slugs. Entomophaga 39, 323–333.CrossRefGoogle Scholar
Symondson, W.O.C. (2002) Diagnostic techniques for determining carabid diets. pp. 111–164in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.Google Scholar
Symondson, W.O.C. (2004) Coleoptera (Carabidae, Staphylinidae, Lampyridae, Drilidae and Silphidae) as predators of terrestrial gastropods. pp. 37–84in Barker, G.M. (Ed.) Natural Enemies of Terrestrial Molluscs. Oxford, UK, CAB International.CrossRefGoogle Scholar
Symondson, W.O.C., Mendis, V.W. & Liddell, J.E. (1995) Monoclonal antibodies for the identification of slugs and their eggs. EPPO Bulletin 25, 377–382.CrossRefGoogle Scholar
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, 741–753.CrossRefGoogle Scholar
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, 137–147.CrossRefGoogle Scholar
Thiele, H.U. (1977) Carabid Beetles in their Environments. Berlin, Germany, Springer Verlag.CrossRefGoogle Scholar
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.Google Scholar
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, 207–216.CrossRefGoogle Scholar
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, 569–579.CrossRefGoogle Scholar
Tod, M.E. (1973) Notes on beetle predators of mollusks. The Entomologist 106, 196–201.Google Scholar
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.Google Scholar
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.Google Scholar
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, 189–197.CrossRefGoogle Scholar
Turin, H., Penev, L., Casale, A., Arndt, E., Assman, T., Makarov, K., Mossakowski, D., Szél, G. & Weber, F. (2003) Species accounts. pp. 151–284in Turin, H., Penev, L. & Casale, A. (Eds) The Genus Carabus in Europe: A Synthesis. Sofia, Bulgaria, Pensoft Publishers.Google Scholar
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, 27–39.Google Scholar
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, 195–203.Google Scholar
Zar, J.H. (1999) Biostatical Analysis, 4th edn. New Jersey, USA, Prentice-Hall.Google Scholar