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

Bulletin of Entomological Research

Volumn 100, Issue 5, 2010, Pages 559-567

  Hatteland, B A ^a   Grutle, K ^b   Mong, C E ^a   Skartveit, J ^c   Symondson, W O C ^d   Solhoy T ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b Student Services   (Norway)

^c Department of Education   (Norway)

^d CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Arion; biological control; Carabidae; Deroceras; invasive species; predation; Staphylinidae

Indexed keywords

BEETLE; BIOCONTROL AGENT; BIOLOGICAL CONTROL; EGG; GASTROPOD; HATCHING; INVASIVE SPECIES; NEMATODE; PESTICIDE; PREDATION; PREY SIZE; SLUG;

ANIMAL; ARTICLE; BEETLE; BIOLOGICAL PEST CONTROL; BODY SIZE; FOOD PREFERENCE; GASTROPOD; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; OOCYTE; PHYSIOLOGY; PREDATION; SPECIES DIFFERENCE;

ANIMALS; BEETLES; BODY SIZE; FOOD PREFERENCES; GASTROPODA; OVUM; PEST CONTROL, BIOLOGICAL; PREDATORY BEHAVIOR; SPECIES SPECIFICITY;

NORWAY;

ARION; ARION LUSITANICUS; ARTHROPODA; CARABIDAE; CARABUS NEMORALIS; COLEOPTERA; DEROCERAS; DEROCERAS RETICULATUM; GASTROPODA; NEBRIA BREVICOLLIS; NEMATODA; PTEROSTICHUS MELANARIUS; PTEROSTICHUS NIGER; STAPHYLINIDAE; STAPHYLINUS;

EID: 78650581428     PISSN: 00074853     EISSN: 14752670     Source Type: Journal    
DOI: 10.1017/S0007485309990629     Document Type: Article

References (59)

1. 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.
2. Anderson, R. (2005) An annotated list of the non-marine Mollusca of Britain and Ireland. Journal of Conchology 38, 607. (Pubitemid 41737864)
3. Asteraki, E.J. (1993) The potential of carabid beetles to control slugs in grass/clover swards. Entomophaga 38, 193-198.
4. 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. (Pubitemid 32763495)
5. Barker, G.M. (2002) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.
6. Bless, R. (1977) Studies on the relationships of carabids as predators to gastropods as prey. Anzeiger für Schadlings-kunde, Pflanzenschutz, Umweltschutz 50, 55-57.
7. 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. (Pubitemid 30354664)
8. Dodd, C.S. (2004) Development and optimisation of PCR-based techniques in predator gut analysis. PhD thesis, Cardiff University, Cardiff, UK.
9. 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. Trond-heim, Norway, Vitenskapsmuseet.
10. Eilenberg, J., Hajek, A. & Lomer, C. (2001) Suggestions for unifying the terminology in biological control. BioControl 46, 387-400. (Pubitemid 34115057)
11. Essl, F. & Rabitsch, W. (2002) Neobiota in Osterreich. Vienna, Austria, Umweltbundesamt
12. 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.
13. Grimm, B., Paill, W. & Kaiser, H. (2000) Daily activities of the pest slug Arion lusitanicus. Journal of Molluscan Studies 66, 125-130. (Pubitemid 30091996)
14. Gruttke, H. (1994) Dispersal of carabid species along a linear sequence of young hedge plantations. pp. 299-303 in Desender, K., Dufrêne, M., Loreau, M., Luff, M.L. & Maelfait, J.-P. (Eds) Carabid Beetles: Ecology and Evolution. Kluwer Academic Publishers.
15. 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.
16. Hengeveld, R. (1980a) Food specialization in ground beetles: an ecological or a phylogenetic process? (Coleoptera, Carabi-dae). Netherlands Journal of Zoology 30, 585-594.
17. Hengeveld, R. (1980b) Qualitative and quantitative aspects of the food of ground beetles (Coleoptera, Carabidae): a review. Netherlands Journal of Zoology, 30, 555-563.
18. Hommay, G. (2002) Agriolimacidae, Arionidae and Milacidae as pests in West European sunflower and maize. pp. 245-254 in Barker, G.M. (Ed.) Molluscs as crop pests. CABI Publishing, Wallingford, UK.
19. 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. (Pubitemid 34286976)
20. 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.
21. 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. (Pubitemid 29211968)
22. 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. (Pubitemid 38300440)
23. Lindroth, C.H. (1985) The Carabidae (Coleoptera) of Fenno-scandia and Denmark. Vol. 1. Fauna Entomologica Scandina-vica 15, 1-225.
24. Lindroth, C.H. (1986) The Carabidae (Coleoptera) of Fenno-scandia and Denmark. Vol. 2. Fauna Entomologica Scandina-vica 15, 226-497.
25. Luff, M.L. (2007) The Carabidae (ground beetles) of Britain and Ireland, 2nd edn. Royal Entomological Society, St Albans, UK.
26. 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. (Pubitemid 32817883)
27. 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. (Pubitemid 32442362)
28. 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.
29. 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.
30. 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. (Pubitemid 36391448)
31. 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. (Pubitemid 36650216)
32. 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.
33. Paill, W. (2004) Slug feeding in the carabid beetle Pterostichus melanarius: seasonality and dependence on prey size. Journal of Molluscan Studies 70, 203-205. (Pubitemid 38583799)
34. 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. (Pubitemid 2082968)
35. 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.
36. 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.
37. 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.
38. 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.
39. South, A. (1992) Terrestrial Slugs: Biology, Ecology and Ccontrol. London, UK, Chapman & Hall.
40. Sunderland, K.D. (2002) Invertebrate pest control of slugs by carabids. pp. 165-214 in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.
41. 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.
42. 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.
43. Symondson, W.O.C. (2002) Diagnostic techniques for determining carabid diets. pp. 111-164 in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.
44. Symondson, W.O.C. (2004) Coleoptera (Carabidae, Staphylini-dae, Lampyridae, Drilidae and Silphidae) as predators of terrestrial gastropods. pp. 37-84 in Barker, G.M. (Ed.) Natural Enemies of Terrestrial Molluscs. Oxford, UK, CAB International.
45. 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.
46. 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. (Pubitemid 27108443)
47. 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.
48. Thiele, H.U. (1977) Carabid Beetles in their Environments. Berlin, Germany, Springer Verlag.
49. 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.
50. 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.
51. 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.
52. Tod, M.E. (1973) Notes on beetle predators of mollusks. The Entomologist 106, 196-201.
53. 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.
54. Tomasga°rd, T.E.H. (2005) Populasjonsdynamikk, nærings- preferansar og reproduksjon/vekst hja° snilen Arion lusi-tanicus 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.
55. 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.
56. Turin, H., Penev, L., Casale, A., Arndt, E., Assman, T., Makarov, K., Mossakowski, D., Szél, G. & Weber, F. (2003) Species accounts. pp. 151-284 in Turin, H., Penev, L. & Casale, A. (Eds) The Genus Carabus in Europe: A Synthesis. Sofia, Bulgaria, Pensoft Publishers.
57. 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 a°rstryck 1996, 27-39.
58. von Proschwitz, T. & Winge, K. (1994) Iberiaskogsnegl-en art pa° spredning i Norge (In Norwegian). 'The Iberian slug-a species expanding in Norway'. Fauna 47, 195-203.
59. Zar, J.H. (1999) Biostatical Analysis, 4th edn. New Jersey, USA, Prentice-Hall.