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The effects of temperature on detection of prey DNA in two species of carabid beetle

Published online by Cambridge University Press:  28 April 2008

K. von Berg*
Affiliation:
Animal Ecology, University of Technology Darmstadt, Schnittspahnstrasse 3, 64287 Darmstadt, Germany
M. Traugott
Affiliation:
Institute of Ecology, Mountain Agriculture Research Unit, University of Innsbruck, Technikerstrasse 25, 6020 Innsbruck, Austria Cardiff School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff CF10 3US, UK
W.O.C. Symondson
Affiliation:
Cardiff School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff CF10 3US, UK
S. Scheu
Affiliation:
Animal Ecology, University of Technology Darmstadt, Schnittspahnstrasse 3, 64287 Darmstadt, Germany
*
*Author for correspondence Fax: +49 6151 166111 E-mail: [email protected]

Abstract

PCR-based techniques to investigate predator-prey trophic interactions are starting to be used more widely, but factors affecting DNA decay in predator guts are still poorly understood. Here, we investigated the effects of time since feeding, temperature and amplicon size on the detectability of prey DNA in the gut content of two closely related predator species. Cereal aphids, Sitobion avenae, were fed to the carabid beetles Pterostichus melanarius and Nebria brevicollis. Beetles were allowed to digest their meal at 12°C, 16°C and 20°C, and batches of beetles were subsequently frozen at time periods from 0–72 h after feeding. Aphid DNA was detected within beetles' gut contents using primers amplifying fragments of 85, 231, 317 and 383 bp. Prey DNA detection rates were significantly higher in N. brevicollis than in P. melanarius, indicating fundamental dissimilarities in prey digestion capacities. High temperatures (20°C) and large amplicons (383 bp) significantly decreased detection rates. The shortest amplicon gave the highest prey DNA detection success, whereas no differences were observed between the 231 bp and the 317 bp fragment. Our results indicate that factors such as ambient temperature, predator taxon and amplicon size should all be considered when interpreting data derived from PCR-based prey detection. Correction for such factors should make calculation of predation rates in the field more accurate and could help us to estimate when predation events occur in the field.

Type
Research Paper
Copyright
Copyright © 2008 Cambridge University Press

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References

Agustí, N., De Vicente, M.C. & Gabarra, R. (1999) Development of sequence amplified characterized region (SCAR) markers of Helicoverpa armigera: a new polymerase chain reaction-based technique for predator gut analysis. Molecular Ecology 8, 14671474.Google Scholar
Anderson, J.F. (1970) Metabolic rates of spiders. Comparative Biochemistry and Physiology 33, 5172.Google Scholar
Chapman, P.A., Armstrong, G. & McKinlay, R.G. (1999) Daily movements of Pterostichus melanarius between areas of contrasting vegetation density within crops. Entomologia Experimentalis et Applicata 91, 477480.CrossRefGoogle Scholar
Chen, Y., Giles, K.L., Payton, M.E. & Greenstone, M.H. (2000) Identifying key cereal aphid predators by molecular gut analysis. Molecular Ecology 9, 18871898.Google Scholar
Cody, R.P. & Smith, J.K. (2006) Applied Statistics and the SAS Programming Language. 445 pp. Upper Saddle River, NJ, Prentice Hall.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, 294299.Google ScholarPubMed
Gariepy, T.D., Kuhlmann, U., Gillott, C. & Erlandson, M. (2007) Parasitoids, predators and PCR: the use of diagnostic molecular markers in biological control of Arthropods. Journal of Applied Entomology 131, 225240.Google Scholar
Greenslade, P.J.M. (1963) Daily rhythms of locomotor activity in some Carabidae (Coleoptera). Entomologia Experimentalis et Applicata 6, 171180.CrossRefGoogle Scholar
Greenstone, M.H. & Hunt, J.H. (1993) Determination of prey antigen half-life in Polistes metricus using a monoclonal antibody-based immunodot assay. Entomologia Experimentalis et Applicata 68, 17.Google Scholar
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, 201209.CrossRefGoogle ScholarPubMed
Hagler, J.R. & Naranjo, S.E. (1997) Measuring the sensitivity of an indirect predator gut content ELISA: Detectability of prey remains in relation to predator species, temperature, time, and meal size. Biological Control 9, 112119.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, 9598.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, 819827.CrossRefGoogle ScholarPubMed
Harwood, J.D, Sunderland, K.D. & Symondson, W.O.C. (2004) Prey selection by linyphiid spiders: molecular tracking of the effects of alternative prey on rates of aphid consumption in the field. Molecular Ecology 13, 35493560.CrossRefGoogle 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, 43904400.CrossRefGoogle ScholarPubMed
Hawkins, J.R. (1997) Finding Mutations, the Basics. 136 pp. Oxford, UK, IRL Press.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, 20592067.CrossRefGoogle ScholarPubMed
Hoogendoorn, M. & Heimpel, G.E. (2002) PCR-based gut content analysis of insect predators: a field study. pp. 9197in van Driesche, R.G. (Ed.) Proceedings of the International Symposium on Biological Control of Arthropods, vol. 1, Morgantown, WV, USA, United States Department of Agriculture, Forest Service.Google Scholar
Ingerson-Mahar, J. (2002) Relating diet and morphology in adult carabid beetles. pp. 111136in Holland, J. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.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, 344352.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, 18721879.Google Scholar
Juen, A. & Traugott, M. (2007) Revealing species-specific trophic links in soil food webs: molecular identification of scarab predators. Molecular Ecology 16, 15451557.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, 947963.CrossRefGoogle ScholarPubMed
Lovei, G.L. & Sunderland, K.D. (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology 41, 231256.Google Scholar
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, 330335.CrossRefGoogle Scholar
Nakamura, M. & Nakamura, K. (1977) Population-dynamics of Chestnut Gall Wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). 5. Estimation of effect of predation by spiders on mortality of imaginal wasps based on precipitin test. Oecologia 27, 97116.CrossRefGoogle Scholar
Read, D.S. (2007) Molecular analysis of subterranean detritivore food webs. PhD thesis, Cardiff University, UK.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, 19631972.Google Scholar
Scheiner, S.M. & Gurevitch, S. (2001) Design and Analysis of Ecological Experiments. 432 pp. New York, Oxford University Press.Google Scholar
Sheppard, S.K. & Harwood, J.D. (2005) Advances in molecular ecology: tracking trophic links through predator-prey food-webs. Functional Ecology 19, 751762.Google Scholar
Sheppard, S.K., Bell, J., Sunderland, K.D., Fenlon, J., Skervin, D. & Symondson, W.O.C. (2005) Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Molecular Ecology 14, 44614468.Google Scholar
Sunderland, K.D. (2002) Invertebrate pest control by carabids. pp. 165214in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.Google Scholar
Sunderland, K.D. & Vickerman, G.P. (1980) Aphid feeding by some polyphagous predators in relation to aphid density in cereal fields. Journal of Applied Ecology 17, 389396.CrossRefGoogle Scholar
Sunderland, K.D., Crook, N.E., Stacey, D.L. & Fuller, B.J. (1987) A study of feeding by polyphagous predators on cereal aphids using ELISA and gut dissection. Journal of Applied Ecology 24, 907933.Google Scholar
Sunderland, K.D., Powell, W. & Symondson, W.O.C. (2005) Populations and communities. pp. 299434in Jervis, M.A. (Ed.) Insects as Natural Enemies: A Practical Perspective. Berlin, Springer.Google Scholar
Symondson, W.O.C. & Liddell, J.E. (1993) Differential antigen decay rates during digestion of molluscan prey by carabid predators. Entomologia Experimentalis et Applicata 69, 277287.CrossRefGoogle Scholar
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627641.Google Scholar
Traugott, M. & Symondson, W.O.C. (2008) Molecular analysis of predation on parasitized hosts. Bulletin of Entomological Research, this issue: 223231.Google Scholar
Williams, G. (1959) Seasonal and diurnal activity of Carabidae, with particular reference to Nebria, Notiophilus and Feronia. Journal of Animal Ecology 28, 309330.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, 20812087.Google Scholar