Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-26T07:21:46.280Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular analysis of predation by carabid beetles (Carabidae) on the invasive Iberian slug Arion lusitanicus

Published online by Cambridge University Press:  23 February 2011

B.A. Hatteland ,
W.O.C. Symondson ,
R.A. King ,
M. Skage ,
C. Schander  and
T. Solhøy
B.A. Hatteland*
Affiliation:
Department of Biology, University of Bergen, Post Box 7803, 5020 Bergen, Norway
W.O.C. Symondson
Affiliation:
Cardiff School of Biosciences, Biomedical Sciences Building, Cardiff University, Museum Avenue, Cardiff, CF10 3AX, UK
R.A. King
Affiliation:
Cardiff School of Biosciences, Biomedical Sciences Building, Cardiff University, Museum Avenue, Cardiff, CF10 3AX, UK
M. Skage
Affiliation:
Department of Biology, University of Bergen, Post Box 7803, 5020 Bergen, Norway
C. Schander
Affiliation:
Department of Biology, University of Bergen, Post Box 7803, 5020 Bergen, Norway
T. Solhøy
Affiliation:
Department of Biology, University of Bergen, Post Box 7803, 5020 Bergen, Norway
*
*Author for correspondence Fax: +47 55584400 E-mail: bjorn.hatteland@bio.uib.no
Get access Rights & Permissions [Opens in a new window]

Abstract

The invasive Iberian slug, Arion lusitanicus, is spreading through Europe and poses a major threat to horticulture and agriculture. Natural enemies, capable of killing A. lusitanicus, may be important to our understanding of its population dynamics in recently invaded regions. We used polymerase chain reaction (PCR) to study predation on A. lusitanicus by carabid beetles in the field. A first multiplex PCR was developed, incorporating species-specific primers, and optimised in order to amplify parts of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene of large Arion slugs, including A. lusitanicus from the gut contents of the predators. A second multiplex PCR, targeting 12S rRNA mtDNA, detected predation on smaller Arion species and the field slug Deroceras reticulatum. Feeding trials were conducted to measure the effects of digestion time on amplicon detectability. The median detection times (the time at which 50% of samples tested positive) for A. lusitanicus and D. reticulatum DNA in the foreguts of Carabus nemoralis were 22 h and 20 h, respectively. Beetle activity-densities were monitored using pitfall traps, and slug densities were estimated using quadrats. Predation rates on slugs in the field by C. nemoralis in spring ranged from 16–39% (beetles positive for slug DNA) and were density dependent, with numbers of beetles testing positive being positively correlated with densities of the respective slug species. Carabus nemoralis was shown to be a potentially important predator of the alien A. lusitanicus in spring and may contribute to conservation biological control.

Keywords

Carabus nemoralisDeroceras reticulatumgut content analysismultiplex PCRpredator-prey interactions
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 6 , December 2011 , pp. 675 - 686
Copyright
Copyright © Cambridge University Press 2011

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

Adis, J. (1979) Problems of interpreting arthropod sampling with pitfall traps. Zoologischer Anzeiger 202, 177–184.Google Scholar
Agusti, N., Shayler, S.P., Harwood, J.D., Vaughan, I.P., Sunderland, K.D. & Symondson, W.O.C. (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Molecular Ecology 12, 3467–3475.CrossRefGoogle ScholarPubMed
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. Acto Oecologia/Oecologia Applicata 3, 387–390.Google Scholar
Anderson, R. (2005) An annotated list of the non-marine Mollusca of Britain and Ireland. Journal of Conchology 38, 607–637.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
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.Google Scholar
Bailey, S.E.R. (2002) Molluscicidal baits for control of terrestrial gastropods. pp. 33–54 in Barker, G.M. (Ed.) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.Google Scholar
Barker, G.M. (2002) Molluscs as Crop Pests. Wallingford, UK, CABI Publishing.CrossRefGoogle Scholar
Begon, M., Harper, J.L. & Townsend, C.R. (2000) Ecology. 3rd edn. Oxford, UK, Blackwell Science.Google 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
Bolker, B.M., Brooks, M.E., Clark, J.C., Geange, S.W., Poulsen, J.R., Stevens, M.H.H. & White, J-S.S. (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24, 127–135.CrossRefGoogle Scholar
Calder, C.R., Harwood, J.D. & Symondson, W.O.C. (2005) Detection of scavenged material in the guts of predators using monoclonal antibodies: a significant source of error in measurement of predation? Bulletin of Entomological Research 95, 57–62.CrossRefGoogle ScholarPubMed
Chen, Y., Giles, K.L., Payton, M.E. & Greenstone, M.H. (2000) Identifying key cereal aphid predators by molecular gut analysis. Molecular Ecology 9, 1887–1898.CrossRefGoogle ScholarPubMed
Chiverton, P.A. (1988) Searching behaviour and cereal aphid consumption by Bembidion lampros and Pterostichus cupreus, in relation to temperature and prey density. Entomologia Experimentalis et Applicata 47, 173–182.CrossRefGoogle Scholar
de Leon, J.H., Fournier, V., Hagler, J.R. & Daane, K.M. (2006) Development of molecular diagnostic markers for sharpshooters Homalodisca coagulata and Homalodisca liturata for use in predator gut content examinations. Entomologia Experimentalis et Applicata 119, 109–119.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. Zoological series, Trondheim, Norway, Vitenskapsmuseet.Google Scholar
Evans, M.E.G. & Forsythe, T.G. (1985) Feeding mechanisms and their variation in form of some adult ground-beetles (Coleoptera: Caraboidea). Journal of Zoology 206, 113–143.CrossRefGoogle 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 ScholarPubMed
Foltan, P., Sheppard, S.K., Konvicka, M. & Symondson, W.O.C. (2005) The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR. Molecular Ecology 14, 4147–4158.CrossRefGoogle ScholarPubMed
Greenstone, M.H., Rowley, D.L., Weber, D.C., Payton, M.E. & Hawthorne, D.J. (2007) Feeding mode and prey detectability half-lives in molecular gut-content analysis: an example with two predators of the Colorado potato beetle. Bulletin of Entomological Research 97, 201–209.CrossRefGoogle ScholarPubMed
Griffith, E., Wratten, S.D. & Vickerman, G.P. (1985) Foraging by the carabid Agonum dorsale in the field. Ecological Entomology 10, 181–189.CrossRefGoogle Scholar
Grimm, B., Paill, W. & Kaiser, H. (2000) Daily activities of the pest slug Arion lusitanicus. Journal of Molluscan Studies 66, 125–130.Google Scholar
Hagley, E.A.C., Holliday, N.J. & Barber, D.R. (1982) Laboratory studies of the food preferences of some orchard carabids (Coleoptera: Carabidae). Canadian Entomologist 114, 431–437.CrossRefGoogle Scholar
Halaj, J., Cady, A.B. & Uetz, G.W. (2000) Modular habitat refugia enhance generalist predators and lower plant damage in soybeans. Environmental Entomology 29, 383–393.CrossRefGoogle Scholar
Hall, T.A. (1999). BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.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 invertebrate predators for multiple prey DNA targets. Molecular Ecology 14, 819–827.Google ScholarPubMed
Harwood, J.D., Desneux, N., Yoo, H.J.S., Rowley, D.L., Greenstone, M.H., Obrycki, J.J. & O'Neil, R.J. (2007) Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Molecular Ecology 16, 4390–4400.Google ScholarPubMed
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.Google ScholarPubMed
Hengeveld, R. (1980a) Polyphagy, oligophagy and food specialisation in ground beetles (Coleoptera, Carabidae). Netherlands Journal of Zoology 30, 564–584.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
Hofsvang, T. (2003) Snegler som skadedyr på planter (Slugs as plant pests). Grønn Kunnskap 7, 10 pp. (in Norwegian).Google Scholar
Holland, J.M. (2002) Agroecology of Carabid Beetles. Andover, UK, Intercept.Google Scholar
Hoogendoorn, M. & Heimpel, G.E. (2001) PCR-based gut content analysis of insect predators: using ribosomal ITS-1 fragments from prey to estimate predation frequency. Molecular Ecology 10, 2059–2067.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Keane, R.M. & Crawley, M.J. (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17, 164–170.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
King, R.A., Moreno-Ripoll, R., Agustí, N., Shayler, S.P., Bell, J.R., Bohan, D.A. & Symondson, W.O.C. (2010a) Multiplex reactions for the molecular detection of predation on pest and non-pest invertebrates in agroecosystems. Molecular Ecology Resources, doi: 10.1111/j.1755-0998.2010.02913.xGoogle Scholar
King, R.A., Vaughan, I.P., Bell, J.R., Bohan, D.A. & Symondson, W.O.C. (2010b) Prey choice by carabid beetles feeding on an earthworm community analysed using species- and lineage-specific PCR primers. Molecular Ecology 19, 1721–1732.CrossRefGoogle 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
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 1. Fauna Entomologica Scandinavica 15, 225 pp.Google Scholar
Luff, M.L. (1982) Population dynamics of Carabidae. Annals of Applied Biology 101, 164–170.Google Scholar
Luff, M.L. (1987) Biology of polyphagous ground beetles in agriculture. Agricultural Zoology Reviews 2, 237–278.Google Scholar
Luff, M.L. (2002) Carabid assemblage organization and species composition. pp. 41–79 in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.Google Scholar
Lövei, G.L. & Sunderland, K.D. (1996) Ecology and behaviour of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology 41, 231–256.CrossRefGoogle ScholarPubMed
Ma, J., Li, D., Keller, M., Schmidt, O. & Feng, X. (2005) A DNA marker to identify predation of Plutella xylostella (Lep., Plutellidae) by Nabis kinbergii (Hem., Nabidae) and Lycosa sp. (Aranaea, Lycosidae). Journal of Applied Entomology 129, 330–335.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
McKemey, A.R., Glen, D.M. & Symondson, W.O.C. (2004) How does a carabid predator find aggregations of slugs in the field? Electroantennograms and behavioural assays suggest chemical cues. Bulletin of Entomological Research 94, 235–244.CrossRefGoogle ScholarPubMed
Mitchell, C.E. & Power, A.G. (2003) Release of invasive plants from fungal and viral pathogens. Nature 421, 625–627.Google ScholarPubMed
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
Paill, W. (2000) Slugs as prey for larvae and imagines of Carabus violaceus L. (Coleoptera, Carabidae). pp. 221–227 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
Paill, W., Backeljau, T., Grimm, B., Kastberger, G. & Kaiser, H. (2002) Isoelectric focusing as a tool to evaluate carabid beetles as predatory agents of the pest slug Arion lusitanicus. Soil Biology and Biochemistry 34, 1333–1342.CrossRefGoogle Scholar
Pakarinen, E. (1994) Autotomy in arionid and limacid slugs. Journal of Molluscan Studies 60, 19–23.CrossRefGoogle Scholar
Pickett, C.H. & Bugg, R.L. (1998) Enhancing Biological Control: Habitat Management to Promote Natural Enemies of Agricultural Pests. Berkeley, USA, University of California Press.Google 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
Read, D.S., Sheppard, S.K., Bruford, M.W., Glen, D.M. & Symondson, W.O.C. (2006) Molecular detection of predation by soil micro-arthropods on nematodes. Molecular Ecology 15, 1963–1972.CrossRefGoogle ScholarPubMed
Rozen, S. & Saletsky, H.J. (1996–1998) PRIMER 3 on the www for general users and for biologist programmers. pp. 365–386 in Krawetz, S. (Ed.) Bioinformatics Methods and Protocols: Methods in Molecular Biology. New Jersey, USA, Humana Press, Totowa.Google Scholar
Spence, J.R. & Niemelä, J.K. (1994) Sampling carabid assemblages with pitfall traps: the madness and the method. Canadian Entomologist 126, 881–894.Google Scholar
Sunderland, K.D. (1996) Progress in quantifying predation using antibody techniques. pp. 419–455 in Symondson, W.O.C. & Liddell, J.E. (Eds) The Ecology of Agricultural Pests, Biochemical Approaches. London, UK, Chapman & Hall.Google Scholar
Sunderland, K.D. (2002) Invertebrate pest control by carabids. pp. 165–214 in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.Google Scholar
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627–641.CrossRefGoogle ScholarPubMed
Symondson, W.O.C. (2004) Coleoptera (Carabidae, Staphylinidae, 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.CrossRefGoogle Scholar
Symondson, W.O.C., Glen, D.M., Wiltshire, 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.Google 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.CrossRefGoogle ScholarPubMed
Szyszko, J., Gryuntal, S. & Schwerk, A. (2004) Differences in locomotory activity between male and female Carabus hortensis (Coleoptera: Carabidae) in a pine forest and a beech forest in relation to feeding state. Environmental Entomology 33, 1442–1446.Google Scholar
Thiele, H.U. (1977) Carabid Beetles in their Environments. Berlin, Germany, Springer Verlag.CrossRefGoogle Scholar
Torchin, M.E., Lafferty, K.D., Doubson, A.P., McKenzie, V.J. & Kuris, A.M. (2003) Introduced species and their missing parasites. Nature 421, 628–630.CrossRefGoogle ScholarPubMed
Traugott, M. & Symondson, W.O.C. (2008) Molecular analysis of predation on parasitized hosts. Bulletin of Entomological Research 98, 223–231.CrossRefGoogle ScholarPubMed
Turin, H., Penev, L., Casale, A., Arndt, E., Assmann, 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.Google Scholar
von Berg, K., Traugott, M., Symondson, W.O.C. & Scheu, S. (2008a) The effects of temperature on detection of prey DNA in two species of carabid beetle. Bulletin of Entomological Research 98, 263–269.CrossRefGoogle ScholarPubMed
von Berg, K., Traugott, M., Symondson, W.O.C. & Scheu, S. (2008b) Impact of abiotic factors on predator-prey interactions: DNA-based gut content analysis in a microcosm experiment. Bulletin of Entomological Research 98, 257–261.CrossRefGoogle Scholar
von Proschwitz, T. (1992) Den spanska skogsnigeln Arion lusitanicus Mabille – en art i snabb spridning med människan i Sverige. Göteborgs Naturhistoriska Museum 1992, 35–42 (with English summary: The Spanish slug Arion lusitanicus Mabille – an anthropochorous slug species spreading rapidly in Sweden).Google Scholar
von Proschwitz, T. (1994) Oxychilus cellarius (Müller) and Oxychilus draparnaudi (Beck) as predators on egg-clutches of Arion lusitanicus Mabille. Journal of Conchology 35, 183–185.Google Scholar
von Proschwitz, T. (1997) Arion lusitanicus Mabille and A. rufus (L.) in Sweden: A comparison of occurrence, spread and naturalization of two alien slug species. Heldia 4, 137–138.Google Scholar
von Proschwitz, T. & Winge, K. (1994) Iberiaskogsnegl - en art på spredning i Norge. (The Iberian slug - a species spreading in Norway.) Fauna 47, 195–203. (in Norwegian).Google Scholar
Weber, F. & Heimbach, U. (2001) Behavioural, reproductive and developmental seasonality in Carabus auronitens and Carabus nemoralis (Col., Carabidae). Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft. Berlin-Dahlem, Germany, Berlin Heft 382.Google Scholar
Winder, L., Hirst, D.J., Carter, N., Wratten, S.D. & Sopp, P.I. (1994) Estimating predation of the grain aphid Sitobion avenae by polyphagous predators. Journal of Applied Ecology 31, 1–12.CrossRefGoogle Scholar
Zaidi, R.H., Jaal, Z., Hawkes, N.J., Hemingway, J. & Symondson, W.O.C. (1999) Can multiple-copy sequences of prey DNA be detected amongst the gut contents of invertebrate predators? Molecular Ecology 8, 2081–2087.CrossRefGoogle ScholarPubMed