Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-27T08:22:49.662Z Has data issue: false hasContentIssue false
  • English
  • Français

Predation by carabid beetles on the invasive slug Arion vulgaris in an agricultural semi-field experiment

Published online by Cambridge University Press:  13 November 2012

E. Pianezzola ,
S. Roth  and
B.A. Hatteland
E. Pianezzola*
Affiliation:
Department of Biology, University of Padova, Padova, Italy
S. Roth
Affiliation:
Bergen Museum, University of Bergen, Bergen, Norway
B.A. Hatteland
Affiliation:
Department of Biology, University of Bergen, Bergen, Norway
*
*Author for correspondence Fax: 0039 0461 653100 E-mail: pianeone@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Arion vulgaris Moquin-Tandon 1855 is one of the most important invasive species in Europe, affecting both biodiversity and agriculture. The species is spreading in many parts of Europe, inflicting severe damage to horticultural plants and cultivated crops partly due to a lack of satisfactory and effective management solutions. Molluscicides have traditionally been used to manage slug densities, although the effects are variable and some have severe side-effects on other biota. Thus, there is a need to explore potential alternatives such as biological control. The nematode Phasmarhabditis hermaphrodita is the only biological agent that has been applied commercially so far. However, other biological control agents such as carabid beetles have also been found to be promising. In addition, some carabid species have been shown to feed on A. vulgaris in the field as well as in the laboratory. Two species in particular have been found to be important predators of A. vulgaris, and these species are also common in agricultural environments: Pterostichus melanarius and Carabus nemoralis. This study is the first to use semi-field experiments in a strawberry field, manipulating densities, to investigate how P. melanarius and C. nemoralis affect densities of A. vulgaris eggs and juveniles, respectively. Gut contents of C. nemoralis were analysed using multiplex PCR methods to detect DNA of juvenile slugs. Results show that both P. melanarius and C. nemoralis significantly affect densities of slug eggs and juvenile slugs under semi-field conditions and that C. nemoralis seems to prefer slugs smaller than one gram. Carabus nemoralis seems to be especially promising in reducing densities of A. vulgaris, and future studies should investigate the potential of using this species as a biological control agent.

Keywords

Arion vulgarisPterostichus melanariusCarabus nemoralissemi-field experimentsjuvenileseggspredation
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 2 , April 2013 , pp. 225 - 232
Copyright
Copyright © Cambridge University Press 2012

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

Allen, R.T. (1979) The occurrence and importance of ground beetles in agricultural and surrounding habitats. pp. 485–505in Erwin, T.L., Ball, G.E. & Whitehead, D.R. (Eds) Carabid Beetles: Their Evolution, Natural History and Classification. The Hague, The Netherlands, W. Junk.Google Scholar
Andersen, A. (1992) Predation by selected carabid and staphylinid species on the aphid Rhopalosiphum padi in laboratory and semi-field experiments. Norwegian Journal of Agricultural Sciences 6, 265–273.Google Scholar
Anderson, R. (2005) An annotated list of the non-marine Mollusca of Britain and Ireland. Journal of Conchology 38, 607–637.Google Scholar
Asteraki, E.J. (1993) The potential of carabid beetles to control slugs in grass/clover swards. Entomophaga 38, 193–198.Google Scholar
Ayre, K. (1995) Evaluation of carabids as predators of slugs in arable land. PhD thesis, University of Newcastle upon Tyne, Newcastle, UK.Google Scholar
Barker, G.M. (1991) Biology of slugs (Agriolimacidae and Arionidae: Mollusca) in New Zealand hill country pastures. Oecologia 85, 581–595.Google Scholar
Barker, G.M. (2002) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.Google Scholar
Bayne, C.J. (1966) Observation of the composition of the layers of the egg of Agriolimax reticulatus, the grey field slug (Pulmonata, Stylomatophora). Comparative Biochemistry and Physiology 19, 317–338.Google Scholar
Bohan, D.A., Bohan, A.C., Glen, D.M., Symondson, W.O.C., Wiltshire, C.W. & Hughes, L. (2001) Spatial dynamics of predation by carabid beetles on slugs. Journal of Animal Ecology 69, 367–379.Google Scholar
Buckland, S.M. & Grime, J.P. (2000) The effects of trophic structure and soil fertility on the assembly of plant communities: a microcosm experiment. Oikos 91, 336–352.Google Scholar
Digweed, S.C. (1994) Detection of mucus-producing prey by Carabus nemoralis Müller and Scaphinotus marginatus. The Coleopterists Bulletin 48, 361–369.Google Scholar
Dodd, C.S. (2004) Development and optimization 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.’ Zoological series. Report, 4, 4–24, Trondheim, Norway, Zoological series, Vitenskapsmuseet.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Glen, D. (2002) Integrated control of slug damage. Pesticide Outlook 13, 137–141.Google Scholar
Greenslade, P.J.M. (1964) Pitfall trapping as a method for studying population of Carabidae (Coleoptera). Journal of Animal Ecology 33, 301–310.Google Scholar
Grimm, B. & Paill, W. (2001) Spatial distribution and home-range of the pest slug Arion lusitanicus (Mollusca: Pulmonata). Acta Oecologica 22, 219–227.Google Scholar
Grimm, B. & Schaumberger, K. (2002) Daily activities of the pest slug Arion lusitanicus under laboratory conditions. Annual of Applied Biology 141, 35–44.Google Scholar
Hammond, R.B. & Byers, R.A. (2002) Agriolimacidae and Arionidae as pests in conservation tillage soybean and maize cropping in North America. pp. 301–314in Barker, G.M. (Ed.) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.Google 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 invertebrates predator for multiple prey DNA targets. Molecular Ecology 14, 819–927.Google Scholar
Hatteland, B.A. (2010) Predation by carabid beetles (Coleoptera, Carabidae) on the invasive Iberian slug Arion lusitanicus. PhD thesis, University of Bergen, Bergen, Norway.Google Scholar
Hatteland, B.A., Grutle, K., Mong, C.E., Skartveit, J., Symondson, W.O.C. & Solhøy, T. (2010) Predation by beetles (Carabidae, Staphylinidae) on eggs and juveniles of the Iberian slug Arion lusitanicus in the laboratory. Bulletin of Entomological Research 100, 559–567.CrossRefGoogle ScholarPubMed
Hatteland, B.A., Symondson, W.O.C., King, R.A., Skage, M., Schander, C. & Solhøy, T. (2011) Molecular analysis of predation by carabid beetles (Carabidae) on the invasive Iberian slug Arion lusitanicus. Bulletin of Entomological Research 101, 675–686.Google Scholar
Holopainen, J.K. & Helenius, J. (1992) Gut contents of ground beetles (Col., Carabidae) and activity of these and other epigeal predators during an outbreak of Rhopalosiphum padi (Hom., Aphididae). Acta Agricolturae Scandinavae, Sect. B: Soil and Plant Scientists 42, 57–61.Google Scholar
Juen, A. & Traugott, M. (2005) Detecting predation and scavenging by DNA gut-content analysis: a case study using a soil insect predator-prey system. Oecologia 142, 344–352.Google Scholar
Juen, A. & Traugott, M. (2006) Amplification facilitators and multiplex PCR: Tools to overcome PCR-inhibition in DNA-gut-content analysis of soil-living invertebrates. Soil Biology & Biochemistry 38, 1872–1879.Google Scholar
King, R.A., Read, D.S., Traugott, M. & Symondson, W.O.C. (2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology 17, 947–963.Google Scholar
Kozłowski, J. (2007) The distribution, biology, population dynamics and harmfulness of Arion lusitanicus Mabille, 1868 (Gastropoda: Pulmonata: Arionidae) in Poland. Journal of Plant Protection Research 47, 219–230.Google Scholar
Kromp, B. (1999) Carabid beetles in sustainable agriculture: a review on pest control efficacy, cultivation impacts and enhancement. Agriculture, Ecosystems and Environment 74, 187–228.Google Scholar
Lang, A. (2000) The pitfalls of pitfalls: a comparison of pitfall trap catches and absolute density estimates of epigeal invertebrate predators in arable land. Anzeiger für Schlädlingskunde /Journal of Pest Science 73, 99–106.Google Scholar
Levesque, C. & Levesque, G.Y. (1994) Abundance and seasonal activity of ground beetles (Coleoptera: Carabidae) in a raspberry plantation and adjacent sites in southern Quebec (Canada). Journal of the Kansas Entomological Society 67, 73–101.Google Scholar
Lindroth, C.H. (1985) The Carabidae (Coleoptera) of Fennoscandia and Denmark. vol. 1. Fauna Entomologica Scandinavica 15, 1–225.Google Scholar
Lindstrom, M.J. & Bates, D.M. (1988) Newton-Raphson and EM Algorithms for Linear Mixed-Effects Models for Repeated-Measures Data. Journal of the American Statistical Association 83, 1014–1022.Google Scholar
Lövei, G.L. & Sunderland, K.D. (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology 41, 231–256.Google Scholar
Luff, M.L. (1975) Some features influencing efficiency of pitfall traps. Oecologia 19, 345–357.Google Scholar
Matalin, A.V. (2004) Geographic variability of the life cycle in Pterostichus melanarius (Coleoptera, Carabidae). Zoologicheskii Zhurnal 85, 573–585.Google 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.Google Scholar
Meenakshi, V.R. & Scheer, B.T. (1969) Chemical studies of the internal shell of the slug, Ariolimax columbianus (Gould) with special reference to the organic matrix. Comparative Biochemistry and Physiology 34, 953–957.Google Scholar
Moens, R. & Glen, D.M. (2002) Agriolimacidae, Arionidae and Milacidae as pests in West European oilseed rape. pp. 425–440in Barker, G.M. (Ed.) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.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.Google Scholar
Pianezzola, E. (2011) Eggs and juveniles predation by carabid beetles on the invasive Iberian slug Arion vulgaris, in agriculture, in Norway. Master's thesis, University of Padua, Padua, Italy.Google Scholar
Pickett, C.H. & Bugg, R.L. (1998) Enhancing Biological Control: Habitat Management to Promote Natural Enemies of Agricultural Pests. Berkeley, CA, USA, University of California Press.Google Scholar
Port, G.R. & Ester, A. (2002) Gastropods as pests in vegetable and ornamental crops in Western Europe. pp. 337–352in Barker, G.M. (Ed.) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.Google Scholar
Quintero, J., Rodriguez-Castro, J., Castillejo, J., Iglesias-Piñeiro, J. & Rey-Méndez, M. (2005) Phylogeny of slug species of the genus Arion: evidence of monophyly of Iberian endemics and of the existence of relict species in Pyrenean refuges. Journal of Zoological Systems 43, 139–148.CrossRefGoogle Scholar
R Development Core Team (2008) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available online at http://www.R-project.org.Google Scholar
Sakovich, N.J. (2002) Integrated management of Cantareus asperses (Müller) (Helicidae) as a pest of citrus in California. pp. 353–360in Barker, G.M. (Ed.) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.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.Google Scholar
Speiser, B., Glen, D., Piggott, S., Ester, A., Davies, K., Castillejo, J. & Coupland, J. (2001) Slug damage and control of slugs in horticultural crop. 1–8, Available online at http://orgprints.org/515/1/Slugcontrol.pdf (accessed 15 August 2012).Google Scholar
Symondson, W.O.C. (1994) The potential of Abax parallelepipedus (col.: Carabidae) for mass breeding as biological control agent against slugs. Entomophaga 39, 323–333.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 Mollusks. Oxford, UK, CABI International.Google Scholar
Symondson, W.O.C., Glen, D.M., Wiltshire, C.W., Langdon, C.J. & Liddel, 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.Google 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(1), 137–147.Google Scholar
Thiele, H.U. (1977) Carabid Beetles in their Environments. Berlin, Germany, Springer Verlag.Google Scholar
Thomas, C.F.G., Parkinson, L. & Marshall, E.J.P. (1998) Isolating the components of activity-density for the carabid beetle Pterostichus melanarius in farmland. Oecologia 116, 103–112.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.Google Scholar
Thomas, R.S., Harwood, J.D., Glen, D.M. & Symondson, W.O.C. (2009) Tracking predator density-dependence and subterranean predation by carabid larvae on slugs using monoclonal antibodies. Ecological Entomology 34, 569–579.Google Scholar
Turin, H., Penev, L., Casale, A., Arndt, E., Assman, T., Makarov, K., Mossakowski, D., Sze´l, 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. (1992) Den spanska skogsnigeln Arion lusitanicus Mabille – en art i snabb spridning med människan i Sverige. (in Swedish). ‘The Spanish slug Arion lusitanicus Mabille – an anthropochorous slug species spreading rapidly in Sweden’. Göteborgs Naturhistoriska Museum 51–59.Google Scholar
von Proschwitz, T. (2008) Snigel - fridstörare i örtagården. Vetenskap och fakta (in Swedish). Bohusläns Museums förlag, Göteborg, Sweden.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
Ward, D.F., New, T.R. & Yen, A.L. (2001) Effects of pitfall trap spacing on the abundance, richness and composition of invertebrate catches. Journal of Insect Conservation 5, 47–53.Google Scholar