Eur. J. Entomol. 111 (5): 631-638, 2014 | DOI: 10.14411/eje.2014.079

Prey detection in carabid beetles (Coleoptera: Carabidae) in woodland ecosystems by PCR analysis of gut contents

Lucija ŠERIĆ JELASKA1, Damjan FRANJEVIĆ1, Sven D. JELASKA1, William O.C. SYMONDSON2
1 Division of Biology, Faculty of Science, University of Zagreb, Rooseveltov trg 6, 10000 Zagreb, Croatia; e-mail: slucija@biol.pmf.hr; dfranjevic@biol.pmf.hr; sven.jelaska@biol.pmf.hr
2 Cardiff School of Biosciences, Cardiff University, The Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX, UK; e-mail: symondson@cardiff.ac.uk

Predatory carabid beetles are important for regulating prey abundance in terrestrial ecosystems. While surveys of carabid diet have revealed many insights into trophic interactions, the high species diversity and heterogeneous developmental stages of prey identified in the gut have made further advances difficult. In addition, the carabid gut contains partially digested and mainly soft tissue parts of the prey species, difficult to identify by traditional methods. Molecular gut content analysis (MGCA) avoids these disadvantages but to date has been limited primarily to revealing pest species in agricultural fields. Here we used MGCA to screen for the presence of Lepidoptera in carabid guts, in woodland ecosystems, in both Croatia and the UK. Data on carabids positive for Lepidoptera were compared with those from previous work on the same carabid assemblages, screened for earthworms, slugs, woodlice and springtails. In both locations, the prey group most frequently detected was earthworms, followed by slugs and Lepidoptera and then finally by woodlice and springtails. The composition of the diet changed with season, carabid sex, and carabid size. In both locations, Lepidoptera were the third most frequent prey, with 27% of carabids testing positive in Croatia and 20% in UK, suggesting that carabids could be significant predators of Lepidoptera in woodland ecosystems and may potentially play an important role in controlling moth pests.

Keywords: Coleoptera, Carabidae, Lepidoptera, molecular gut content analyses, soil fauna, woodland

Received: December 16, 2013; Revised: August 1, 2014; Accepted: August 1, 2014; Prepublished online: September 10, 2014; Published: December 10, 2014  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
ŠERIĆ JELASKA, L., FRANJEVIĆ, D., JELASKA, S.D., & SYMONDSON, W.O.C. (2014). Prey detection in carabid beetles (Coleoptera: Carabidae) in woodland ecosystems by PCR analysis of gut contents. EJE111(5), 631-638. doi: 10.14411/eje.2014.079
Download citation

References

  1. Boreau de Roince C., Lavigne C., Ricard J., Franck P., Bouvier J., Garcin A. & Symondson W.O.C. 2012: Predation by generalist predators on the codling moth versus a closely-related emerging pest the oriental fruit moth: a molecular analysis. - Agric. Forest Entomol. 14: 260-269 Go to original source...
  2. Day K.R. & Leather S.R. 1997: Threats for forestry by insect pests in Europe. In Watt A.D., Stork N.E. & Hunter M.D. (eds): Forests and Insects. Chapman & Hall, London, pp. 177-205
  3. Dennison D.F. & Hodkinson I.D. 1983: Structure of the predatory beetle community in a woodland soil ecosystem. I. Prey Selection. - Pedobiologia 25: 109-115 Go to original source...
  4. Dodd C.S. 2004: Development and Optimisation of PCR-based Techniques in Predator Gut Snalysis. PhD thesis, Cardiff University, UK, 267 pp
  5. Dodd L.E., Lacki M.J. & Rieske L.K. 2008: Variation in moth occurrence and implications for foraging habits of Ozark big-eared bats. - Forest Ecol. Manag. 255: 3866-3872 Go to original source...
  6. Folmer O., Black M., Hoeh W., Lutz R. & Vrijenhoek R. 1994: DNA primers for amplification of mitochondrial cytochrome coxidase subunit I from diverse metazoan invertebrates. - Mol. Marine Biol. Biotechnol. 3: 294-299
  7. Freude H., Harde K.W., Lohse G.A. & Klausnitzer B. 2004: Die Kaefer Mitteleuropas. Band 2. Spectrum, Elsevier, Muenchen, 521 pp
  8. Foltan P. 2004: Influence of slug defence mechanisms on the prey preferences of the carabid predator Pterostichus melanarius (Coleoptera: Carabidae). - Eur. J. Entomol. 101: 359-364 Go to original source...
  9. Forbes S.A. 1883: The food relationships of the Carabidae and Coccinellidae. - Ill. St. Lab. Nat. Hist. Bull. 1: 33-64 Go to original source...
  10. 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. - Mol. Ecol. 14: 819-827 Go to original source...
  11. Hatteland B.A., Grutle K., Mong C.E., Skartveit J., Symondson W.O.C. & Solhoy T. 2010: Predation by beetles (Carabidae, Staphylinidae) on eggs and juveniles of the Iberian slug Arion lusitanicus in the laboratory. - Bull. Entomol. Res. 100: 559-567 Go to original source...
  12. Hatteland B.A., Haukeland S., Roth S., Brurberg M.B., Vaughan I.P. & Symondson W.O.C. 2013: Spatiotemporal analysis of predation by carabid beetles (Carabidae) on nematode infected and uninfected slugs in the field. - PLoS ONE 8(12): eB2142. doi:10.1371/jounal.pone.0082142 Go to original source...
  13. Hatteland B.A., Symondson W.O.C., King R.A., Skage M., Schander C. & Solhoy T. 2011: Molecular analysis of predation by carabid beetles (Carabidae) on the invasive Iberian slug Arion lusitanicus. - Bull. Entomol. Res. 101: 675-686 Go to original source...
  14. Heisswolf A., Klemola N., Ammunet T. & Klemola T. 2009: Responses of generalist invertebrate predators to pupal densities of autumnal and winter moths under field conditions. - Ecol. Entomol. 34: 709-717 Go to original source...
  15. Hengeveld R. 1980a: Polyphagy, oligophagy and food specialization in ground beetles (Coleoptera, Carabidae). - Neth. J. Zool. 30: 564-584 Go to original source...
  16. Hengeveld R. 1980b: Food specialization in ground beetles (Coleoptera, Carabidae): An ecological or a phylogenetic process? - Neth. J. Zool. 30: 585-594 Go to original source...
  17. Hengeveld R. 1985: Methodology of explaining differences in dietary composition of carabid beetles by competition. - Oikos 45: 37-49 Go to original source...
  18. Jarman S.N., Redd K.S. & Gales N.J. 2006: Group-specific primers for amplifying DNA sequences that identify Amphipoda, Cephalopoda, Echinodermata, Gastropoda, Isopoda, Ostracoda and Thoracica. - Mol. Ecol. Notes 6: 268-271 Go to original source...
  19. Jeffery S., Gardi C., Jones A., Montanarella L., Marmo L., Miko L., Ritz K., Peres G., Roembke J. & van der Putten W. 2010: European Atlas of Soil Biodiversity. Publications Office of the European Union, Luxembourg, 128 pp
  20. King R.A., Vaughan I.P., Bell J.R., Bohan D.A. & Symondson W.O.C. 2010: Prey choice by carabid beetles feeding on an earthworm community analysed using species- and lineage-specific PCR primers. - Mol. Ecol. 19: 1721-1732 Go to original source...
  21. Kuusk A.K. & Agusti N. 2008: Group-specific primers for DNA-based detection of springtails (Hexapoda: Collembola) within predator gut contents. - Mol. Ecol. Resour. 8: 678-681 Go to original source...
  22. Luff M.L. 2007: The Carabidae (Ground Beetles) of Britain and Ireland. Handbooks for the Identification of British Insects. Vol. 4, Part 2. 2nd ed. Royal Entomological Society, St. Albans & Field Studies Council, Shrewsbury, 247 pp
  23. McKemey A.R., Symondson W.O.C., Glen D.M. & Brain P. 2001: Effect of slug size on predation by Pterostichus melanarius (Coleoptera: Carabidae). - Biocontr. Sci. Technol. 11: 83-93 Go to original source...
  24. 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. - Bull. Entomol. Res. 93: 227-234 Go to original source...
  25. Niemelae J., Haila Y., Halme E., Pajunen T. & Punttila P. 1989: The annual activity cycle of carabid beetles in the southern Finnish taiga. - Ann. Zool. Fenn. 26: 35-41
  26. Paill W. 2000: Slugs as a prey for larvae and imagines of Carabus violaceus L. (Coleoptera, Carabidae). In Brandmaye P., Lovei G.L., Brandmayr T.Z., Casale A. & Vigna Taglianti A. (eds): Natural History and Applied Ecology of Carabid Beetles. Pensoft, Sofia, pp. 221-222
  27. Paill W. 2004: Slug feeding in the carabid beetle Pterostichus melanarius: seasonality and dependence on prey size. - J. Mollusc. Stud. 70: 203-205 Go to original source...
  28. Seric Jelaska L., Jurasovic J., Brown S.D., Vaughan P.I. & Symondson W.O.C. 2014: Molecular field analysis of trophic relationships in soil-dwelling invertebrates to identify mercury, lead and cadmium transmission through forest ecosystems. - Mol. Ecol. 23: 3755-3766 Go to original source...
  29. Sunderland K.D. 1975: The diet of some predatory arthropods in cereal crops. - J. Appl. Ecol. 12: 389-396 Go to original source...
  30. Sutherland R.M. 2000: Molecular Analysis of Avian Diets. PhD Thesis, University of Oxford, 180 pp
  31. 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 reeding state. - Environ. Entomol. 33: 1442-1446 Go to original source...
  32. Symondson W.O.C., Glen D.M., Erickson M.L., Liddell J.E. & Langdon C.J. 2000: Do earthworms help to sustain the slug predator Pterostichus melanarius (Coleoptera: Carabidae)within crops? Investigations using monoclonal antibodies. - Mol. Ecol. 9: 1279-1292 Go to original source...
  33. Symondson W.O.C., Cesarini S., Dodd P.W., Harper G.L., Bruford M.W., Glen D.M., Wiltshire C.W. & Harwood J.D. 2006: Biodiversity vs. biocontrol: positive and negative effects of alternative prey on control of slugs by carabid beetles. - Bull. Entomol. Res. 96: 637-645 Go to original source...
  34. Thiele H.U. 1977: Carabid Beetles in their Environments. Springer, Berlin, Heidelberg, New York, 369 pp Go to original source...
  35. Traugott M., Bell J.R., Raso L., Sint D. & Symondson W.O.C. 2012: Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation. - Bull. Entomol. Res. 102: 239-247 Go to original source...
  36. Tyler G. 2012: Difference in male : female ratio among species od the genus Crabus L. (Coleoptera: Carabidae) in south Sweden. - Baltic J. Coleopterol. 12: 167-174
  37. 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. - Bull. Entomol. Res. 98: 257-261 Go to original source...
  38. Weseloh R.M. 1985: Predation by Calosoma sycophanta L. (Coleoptera, Carabidae) evidence for a large impact on gypsy moth Lymantria dispar pupae. - Can. Entomol. 117: 1117-1126 Go to original source...
  39. Weseloh R.M. 1988: Prey preferences of Calosoma sycophanta L. (Coleoptera: Carabidae) larvae and relationship of prey consumption to predator size. - Can. Entomol. 120: 873-880 Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.