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Molecular analysis of predation on parasitized hosts

Published online by Cambridge University Press:  28 April 2008

M. Traugott  and
W.O.C. Symondson
M. Traugott*
Affiliation:
Cardiff School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff CF10 3US, UK Institute of Ecology, Mountain Agriculture Research Unit, University of Innsbruck, Technikerstrasse 25, 6020 Innsbruck, Austria
W.O.C. Symondson
Affiliation:
Cardiff School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff CF10 3US, UK
*
*Author for correspondence Fax: +43 512 507 6190 E-mail: Michael.Traugott@uibk.ac.at
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Abstract

Predation on parasitized hosts can significantly affect natural enemy communities, and such intraguild predation may indirectly affect control of herbivore populations. However, the methodological challenges for studying these often complex trophic interactions are formidable. Here, we evaluate a DNA-based approach to track parasitism and predation on parasitized hosts in model herbivore-parasitoid-predator systems. Using singleplex polymerase chain reaction (SP-PCR) to target mtDNA of the parasitoid only, and multiplex PCR (MP-PCR) to additionally target host DNA as an internal amplification control, we found that detection of DNA from the parasitoid, Lysiphlebus testaceipes, in its aphid host, Aphis fabae, was possible as early as 5 min. post parasitism. Up to 24 h post parasitism SP-PCR proved to be more sensitive than MP-PCR in amplifying parasitoid DNA. In the carabid beetles Demetrias atricapillus and Erigone sp. spiders, fed with aphids containing five-day-old parasitoids, parasitoid and aphid DNA were equally detectable in both predator groups. However, when hosts containing two-day-old parasitoids were fed to the predators, detection of parasitoid prey was possible only at 0 h (immediately after consumption) and up to 8 h post consumption in carabids and spiders, respectively. Over longer periods of time, post-feeding prey detection success was significantly higher in spiders than in carabid beetles. MP-PCR, in which parasitoid and aphid DNA were simultaneously amplified, proved to be less sensitive at amplifying prey DNA than SP-PCR. In conclusion, our study demonstrates that PCR-based parasitoid and prey detection offers an exciting approach to further our understanding of host-parasitoid-predator interactions.

Keywords

trophic interactionsintraguild predationparasitoidsgeneralist predatorsLysiphlebus testaceipesAphis fabaediagnostic PCR
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 3 , June 2008 , pp. 223 - 231
Copyright
Copyright © 2008 Cambridge University Press

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References

Admassu, B., Juen, A. & Traugott, M. (2006) Earthworm primers for DNA-based gut content analysis and their cross-reactivity in a multi-species system. Soil Biology and Biochemistry 38, 1308–1315.CrossRefGoogle Scholar
Anderson, J.F. (1970) Metabolic rates in spiders. Comparative Biochemistry and Physiology 33, 51–72.CrossRefGoogle ScholarPubMed
Brodeur, J. & Rosenheim, J.A. (2000) Intraguild interactions in aphid parasitoids. Entomologia Experimantalis et Applicata 97, 93–108.CrossRefGoogle Scholar
Colfer, R.G. & Rosenheim, J.A. (2001) Predation on immature parasitoids and its impact on aphid suppression. Oecologia 126, 292–304.CrossRefGoogle ScholarPubMed
Deagle, B.E., Eveson, J.P. & Jarman, S.N. (2006) Quantification of damage in DNA recovered from highly degraded samples – a case study on DNA in faeces. Frontiers in Zoology 3, doi: 10.1186/1742-9994-3-11CrossRefGoogle ScholarPubMed
Dytham, C. (2003) Choosing and Using Statistics: A Biologist's Guide. 2nd edn.248 pp. Malden, MA, Blackwell Publishing.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 ScholarPubMed
Foltan, P., Sheppard, S., 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
Gariepy, T.D., Kuhlmann, U., Haye, T., Gillott, C. & Erlandson, M. (2005) A single-step muliplex PCR assay for the detection of European Peristenus spp., parasitoids of Lygus spp. Biocontrol Science and Technology 15, 481–495.CrossRefGoogle Scholar
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, 225–240.CrossRefGoogle Scholar
Greenstone, M.H. (2006) Molecular methods for assessing insect parsitism. Bulletin of Entomological Research 96, 1–13.CrossRefGoogle Scholar
Greenstone, M.H. & Bennett, A.F. (1980) Foraging strategy and metabolic rate in spiders. Ecology 61, 1255–1259.CrossRefGoogle 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, 201–209.CrossRefGoogle ScholarPubMed
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
Hardee, D.D., O'Brian, P.J., Elzen, G.W. & Snodgrass, G.L. (1990) Emergence and survival of the parasitoid Lysiphlebus testaceipes from Aphis gossypii exposed to aphicides. Southwestern Entomologist 15, 211–216.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.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, 3549–3560.CrossRefGoogle ScholarPubMed
Hawkins, J.R. (1997) Finding Mutations. 136 pp. Oxford, IRL Press.Google Scholar
Jervis, M.A. & Copland, M.J.W. (1996) The life cycle. pp. 63–161in Jervis, M.A. & Kidd, N. (Eds) Insects as Natural Enemies: Practical Approaches to Their Study and Evaluation. New York, Chapman & Hall.CrossRefGoogle Scholar
Jones, D.B., Giles, K.L., Chen, Y. & Shufran, K.A. (2005) Estimation of hymenopteran parasitism in cereal aphids by using molecular markers. Journal of Economic Entomology 98, 217–221.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
Juen, A. & Traugott, M. (2007) Revealing species-specific trophic links in below-ground invertebrate communities: The predator guild of scarab larvae identified by diagnostic PCR. Molecular Ecology 16, 1545–1557.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
Lumbierres, B., Stary, P. & Pons, X. (2007) Seasonal parasitism of cereal aphids in a Mediterranean arable crop system. Journal of Pest Science 80, 125–130.CrossRefGoogle Scholar
Meyhofer, R. (2001) Intraguild predation by aphidophagous predators on parasitised aphids: the use of multiple video cameras. Entomologia Experimentalis et Applicata 100, 77–87.CrossRefGoogle Scholar
Nyffeler, M. & Sunderland, K.D. (2003) Composition, abundance and pest control potential of spider communities in agroecosystems: a comparison of European and US studies. Agriculture Ecosystems & Environment 95, 579–612.CrossRefGoogle Scholar
Persad, A.B., Jeyaprakash, A. & Hoy, M.A. (2004) High fidelity PCR assay discrimainates between immature Lipolexis oregmae and Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) within their aphid hosts. Florida Entomologist 87, 18–24.CrossRefGoogle Scholar
Pike, K.S., Stary, P., Miller, T., Graf, G., Allison, D., Boydston, L. & Miller, R. (2000) Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Northwest USA. Proceedings of the Entomological Society of Washington 102, 688–740.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
Rosenheim, J.A. (1998) Higher-order predators and the regulation of insect herbivore populations. Annual Review of Entomology 43, 421–447.CrossRefGoogle ScholarPubMed
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, 4461–4468.CrossRefGoogle ScholarPubMed
Snyder, W.E. & Ives, A.R. (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82, 705–716.CrossRefGoogle Scholar
Stary, P., Lyon, J.P. & Leclant, F. (1988) Biocontrol of aphids by the introduced Lysiphlebus testaceipes (Cress.) (Hym., Aphidiidae) in Mediterranean France. Journal of Applied Entomology 105, 74–87.CrossRefGoogle Scholar
Sunderland, K.D. & Vickerman, G.P. (1980) Aphid feeding by polyphagous predators in relation to aphid density in cereal fields. Journal of Applied Ecology 17, 389–396.CrossRefGoogle Scholar
Sunderland, K.D., Axelsen, J.A., Dromph, K., Freier, B., Hemptinne, J.-L., Holst, N.H., Mols, P.J.M., Petersen, M.K., Powell, W., Ruggle, P., Triltsch, H. & Winder, L. (1997) Pest control by a community of natural enemies. Acta Jutlandica 72, 271–326.Google Scholar
Sunderland, K.D., Powell, W. & Symondson, W.O.C. (2005) Populations and communities. pp. 299–434in Jervis, M.A. (Ed.) Insects as Natural Enemies: A Practical Perspective. Berlin, Springer.CrossRefGoogle Scholar
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627–641.CrossRefGoogle ScholarPubMed
Traugott, M., Zangerl, P., Juen, A., Schallhart, N. & Pfiffner, L. (2006) Detecting key parasitoids of lepidopteran pests by multiplex PCR. Biological Control 39, 39–46.CrossRefGoogle Scholar
von Berg, K., Traugott, M., Symondson, W.O.C. & Scheu, S. (2008) The effects of temperature on detection of prey DNA in two species of carabid beetle. Bulletin of Entomological Research, this issue: 263–269.Google Scholar
Walton, M.P., Loxdale, H.D. & Williams, L.A. (1990a) Electrophoretic keys for the identification of parasitoids (Hymenoptera, Braconidae, Aphelinidae) attacking Sitobion avenae (F.) (Hemiptera, Aphididae). Biological Journal of the Linnaean Society 40, 333–346.CrossRefGoogle Scholar
Walton, M.P., Powell, W., Loxdale, H.D. & Williams, L.A. (1990b) Electrophoresis as a tool for estimating levels of hymenopterous parasitism in field populations of the cereal aphid, Sitobion avenae. Entomologia Experimentalis et Applicata 54, 271–279.CrossRefGoogle Scholar
Weathersbee, A.A., Shufran, K.A., Panchal, T.D., Dang, P.M. & Evans, G.A. (2004) Detection and differentiation of parasito ids (Hymenoptera: Aphidiidae and Aphelinidae) of the brown citrus aphid (Homoptera: Aphididae): Species-specific polymerase chain reaction amplification of 18S rDNA. Annals of the Entomological Society of America 97, 286–292.CrossRefGoogle Scholar
Zhu, Y.C., Riddick, E.W., Williams, I.L., Schotzko, D.J., Logarzo, G.A. & Jackson, C.G. (2004) Potential of detection and identification of nymphal parasitoids (Hymenoptera: Braconidae) of Lygus Bugs (Heteroptera: Miridae) by using polymerase chain reaction and ITS2 sequence analysis techniques. Annals of the Entomological Society of America 97, 743–752.CrossRefGoogle Scholar