Skip to main content

Advertisement

SpringerLink
Log in

Detecting arthropod intraguild predation in the field

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The process of biological control carries a distinct risk that an alien biological control agent (BCA) will become established as an invasive alien species with an associated threat to the local ecosystem biodiversity. It is imperative that a wide-ranging environmental risk assessment (ERA) is performed before the release of any BCA. This should include considering various potential but difficult to observe ecological interactions between the BCA and members of the native community, including disruption of intraguild relationships. Detection of intraguild predation (IGP) events involving predatory arthropods in the field can be done by analyzing their gut contents. Polymerase chain reaction (PCR) is a sensitive and specific tool to identify target prey DNA within a predator’s gut. This paper reviews the efficiency of a DNA based approach for detecting IGP in the field, compared with detection by the use of monoclonal antibodies or gas chromatography. Prey specificity, detection times after prey consumption, capacity for quantification, multiple prey targeting and the time and costs involved in developing and using the different methods are considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Adriaens T, San Martin G, Hautier L, Branquart E, Maes D (2010) Toward a Noah’s Ark for native ladybirds in Belgium? IOBC/WPRS Bull 58:1–3

    Google Scholar 

  • Agustí N, Shayler SP, Harwood JD, Vaughan IP, Sunderland KD, Symondson WO (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Mol Ecol 12:3467–3475

    Article  PubMed  Google Scholar 

  • Arim M, Marquet PA (2004) Intraguild predation: a widespread interaction related to species biology. Ecol Lett 7:557–564

    Article  Google Scholar 

  • Becerro MA, Starmer JA, Paul VJ (2006) Chemical defenses of cryptic and aposematic gastropterid molluscs feeding on their host sponge Dysidea granulosa. J Chem Ecol 32:1491–1500

    Article  CAS  PubMed  Google Scholar 

  • Berkvens N, Bonte J, Berkvens D, Deforce K, Tirry L, De Clercq P (2008) Pollen as an alternative food for Harmonia axyridis. BioControl 53:201–210

    Article  Google Scholar 

  • Bigler F, Babendreier D, Kuhlmann U (2006) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI Publishing, Wallingford

    Book  Google Scholar 

  • Boreham PFL, Ohiagu CE (1978) The use of serology in evaluating invertebrate prey-predator relationships: a review. B Entomol Res 68:171–194

    Article  Google Scholar 

  • Brown PMJ, Frost R, Doberski J, Sparks T, Harrington R, Roy HE (2011a) Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol Entomol 36:231–240

    Article  Google Scholar 

  • Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Lawson Handley LJ (2011b) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl. doi:10.1007/s10526-011-9379-1

  • Chen Y, Giles KL, Payton ME, Greenstone MH (2000) Identifying key cereal aphid predators by molecular gut analysis. Mol Ecol 9:1887–1898

    Article  CAS  PubMed  Google Scholar 

  • Daloze D, Braekman J-C, Pasteels JM (1995) Ladybird defence alkaloids: structural, chemotaxonomic and biosynthetic aspects (Col.: Coccinellidae). Chemoecology 5(6):173–183

    Google Scholar 

  • De Clercq P, Bale JS (2011) Risks of invertebrate biological control agents—Harmonia axyridis as a case study. In: Ehlers RU (ed) Regulations of biological control agents. Springer, Dordrecht, pp 243–255

    Chapter  Google Scholar 

  • De Clercq P, Mason PG, Babendreier D (2011) Benefits and risks of exotic biological control agents. BioControl. doi:10.1007/s10526-011-9372-8

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for the amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Foltan P, Sheppard S, Konvicka M, Symondson WO (2005) The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR. Mol Ecol 14:4147–4158

    Article  CAS  PubMed  Google Scholar 

  • Fournier V, Hagler JR, Daane KM, de León JH, Groves RL, Costa HS, Henneberry TJ (2006) Development and application of a glassy-winged and smoke-tree sharpshooter egg-specific predator gut content ELISA. Biol Control 37:108–118

    Article  CAS  Google Scholar 

  • Galvan TL, Burkness EC, Hutchison WD (2007) Enumerative and binomial sequential sampling plans for the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in wine grapes. J Econ Entomol 100:1000–1010

    Article  CAS  PubMed  Google Scholar 

  • Gardiner MM, Landis DA (2007) Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies. Biol Control 40:386–395

    Article  Google Scholar 

  • Gibbs M, Schönrogge K, Alma A, Melika G, Quacchia A, Stone GN, Aebi A (2011) Torymus sinensis: a viable management option for the biological control of Dryocosmus kuriphilus in Europe? BioControl. doi:10.1007/s10526-011-9364-8

  • Greenstone MH (1996) Serological analysis of arthropod predation: past, present and future. In: Symondson WOC, Liddell JE (eds) The ecology of agricultural pests: biochemical approaches. Chapman & Hall, London, pp 265–300

    Google Scholar 

  • Greenstone MH, Rowley DL, Weber DC, Payton ME, Hawthorne DJ (2007) Feeding mode and prey detectability half-lives in molecular gut-content analysis: an example with two predators of the Colorado potato beetle. B Entomol Res 97:201–209

    Article  CAS  Google Scholar 

  • Harper GL, King RA, Dodd CS, Harwood JD, Glen DM, Bruford MW, Symondson WOC (2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Mol Ecol 14:819–828

    Article  CAS  PubMed  Google Scholar 

  • Harwood JD, Greenstone MH (2008) Molecular diagnosis of natural enemy-host interactions. In: Liu N (ed) Recent advances in insect physiology. Toxicology and molecular biology. Research Signpost, Kerala, pp 41–57

    Google Scholar 

  • Harwood JD, Obrycki JJ (2005) Quantifying aphid predation rates of generalist predators in the field. Eur J Entomol 102:335–350

    Article  Google Scholar 

  • Harwood JD, Phillips SW, Sunderland KD, Symondson WOC (2001) Secondary predation: quantification of food chain errors in an aphid-spider-carabid system using monoclonal antibodies. Mol Ecol 10:2049–2057

    Article  CAS  PubMed  Google Scholar 

  • Harwood JD, Desneux N, Yoo HJS, Rowley DL, Greenstone MH, Obrycki JJ, O′Neil RJ (2007) Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Mol Ecol 16(20):4390–4400

    Article  CAS  PubMed  Google Scholar 

  • Hautier L, Grégoire J-C, de Schauwers J, San Martin G, Callier P, Jansen J-P, De Biseau J-C (2008) Intraguild predation by Harmonia axyridis on coccinellids revealed by exogenous alkaloid sequestration. Chemoecology 18:191–196

    Article  CAS  Google Scholar 

  • Hautier L, San Martin G, Callier P, de Biseau JC, Gregoire JC (2011) Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biol Invasions. doi:10.1007/s10530-010-9935-0

  • Holway DA, Lach L, Suarez A, Tsutsui N, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233

    Article  Google Scholar 

  • Hoogendoorn M, Heimpel GE (2001) PCR-based gut content analysis of insect predators: using ribosomal ITS-1 fragments from prey to estimate predation frequency. Mol Ecol 10:2059–2067

    Article  CAS  PubMed  Google Scholar 

  • Hoy MA (1994) Insect molecular genetics: an introduction to principals and applications. Academic Press, San Diego, California

    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 142:344–352

    Article  PubMed  Google Scholar 

  • Kajita Y, Obrycki JJ, Sloggett JJ, Haynes KF (2010) Intraspecific alkaloid variation in ladybird eggs and its effects on con- and hetero-specific intraguild predators. Oecologia 163:313–322

    Article  PubMed  Google Scholar 

  • Kasper ML, Reeson AF, Cooper SJB, Perry KD, Austin AD (2004) Assessment of prey overlap between a native (Polistes humilis) and an introduced (Vespula germanica) social wasp using morphology and phylogenetic analyses of 16S rDNA. Mol Ecol 13:2037–2048

    Article  CAS  PubMed  Google Scholar 

  • Kenis M, Auger-Rozenberg MA, Roques A, Timms L, Péré C, Cock MJW, Settele J, Augustin S, Lopez-Vaamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45

    Article  Google Scholar 

  • King RA, Read DS, Traugott M, Symondson WOC (2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Mol Ecol 17:947–963

    Article  CAS  PubMed  Google Scholar 

  • Kiritani K, Dempster JP (1973) Different approaches to the quantitative evaluation of natural enemies. J Appl Ecol 10:323–330

    Google Scholar 

  • Knutsen H, Vogt NB (1985) An approach to identifying the feeding patterns of lobsters using chemical analysis and pattern recognition by the method of SIMCA I. Identification of a prey organism Artemza salzna (L.) in the stomachs of juvenile lobsters Homarus gammarus (L.). J Exp Mar Biol Ecol 89:109–119

    Article  Google Scholar 

  • Lawson Handley JL, Estoup A, Thomas C, Lombaert E, Facon B, Aebi A, Evans D, Roy HE (2011) Ecological genetics of invasive species. BioControl. doi:10.1007/s10526-011-9386-2

  • Leibhold AM, Work TT, McCullough DD, Cavey JF (2006) Airline baggage as a pathway for alien insect species invading the United States. Am Entomol 52:48–54

    Article  Google Scholar 

  • McMillan S, Kuusk A-K, Cassel-Lundhagen A, Ekbom B (2007) The influence of time and temperature on molecular gut content analysis: Adalia bipunctata fed with Rhopalosiphum padi. Insect Sci 14:353–358

    Article  CAS  Google Scholar 

  • Moser SE, Harwood JD, Obrycki JJ (2008) Interaction pathways between Diptera and coccinellid larvae: evidence from an antibody-based detection system. http://esa.confex.com/esa/2008/techprogram/paper_37704.htm

  • Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53:147–168

    Article  Google Scholar 

  • Pickering GJ, Lin J, Riesen R, Reynolds A, Brindle I, Soleas G (2004) Influence of Harmonia axyridis on the sensory properties of white and red wine. Am J Enol Vitic 55:153–159

    Google Scholar 

  • Polis GA, Holt RD (1992) Intraguild predation—the dynamics of complex trophic interactions. Trends Ecol Evol 7(5):151–154

    Article  CAS  PubMed  Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation—potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330

    Article  Google Scholar 

  • Pons J (2006) DNA-based identification of preys from nondestructive, total DNA extractions of predators using arthropod universal primers. Mol Ecol Notes 6:623–626

    Article  CAS  Google Scholar 

  • Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jafee BA (1995) Intraguild predation among biological control agents: theory and evidence. Biol Control 5:303–335

    Article  Google Scholar 

  • Roy HE, Wajnberg E (2008a) From biological control to invasion: the ladybird Harmonia axyridis as a model species. Springer, Dordrecht

    Book  Google Scholar 

  • Roy HE, Wajnberg E (2008b) From biological control to invasion: the ladybird Harmonia axyridis as a model species. BioControl 53:1–4

    Article  Google Scholar 

  • Sheppard SK, Harwood JD (2005) Advances in molecular ecology: tracking trophic links through predator–prey food-webs. Funct Ecol 19:751–762

    Article  Google Scholar 

  • Sheppard SK, Bell J, Sunderland KD, Fenlon J, Skervin D, Symondson WOC (2005) Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Mol Ecol 14:4461–4468

    Article  CAS  PubMed  Google Scholar 

  • Sloggett JJ, Davis AJ (2010) Eating chemically defended prey: alkaloid metabolism in an invasive ladybird predator of other ladybirds (Coleoptera: Coccinellidae). J Exp Biol 213:237–241

    Article  CAS  PubMed  Google Scholar 

  • Sloggett JJ, Obrycki JJ, Haynes KF (2009) Identification and quantification of predation: novel use of gas chromatography-mass spectrometric analysis of prey alkaloid markers. Funct Ecol 23:416–426

    Article  Google Scholar 

  • Sloggett JJ, Magro A, Verheggen FJ, Hemptinne J-L, Hutchison WD, Riddick EW (2011) The chemical ecology of Harmonia axyridis. BioControl. doi:10.1007/s10526-011-9376-4

  • Sopp PI, Sunderland KD (1989) Some factors affecting the detection period of aphid remains in predators using ELISA. Entomol Exp Appl 51:11–20

    Article  Google Scholar 

  • Sopp PI, Sunderland KD, Fenlon JS, Wratten SD (1992) An improved quantitative method for estimating invertebrate predation in the field using an enzyme-linked immunosorbent assay (ELISA). J Appl Ecol 29:295–302

    Article  Google Scholar 

  • Sunderland KD (1988) Quantitative methods for detecting invertebrate predation in the field. Ann Appl Biol 112:201–224

    Article  Google Scholar 

  • Symondson WOC (2002) Molecular identification of prey in predator diets. Mol Ecol 11:627–641

    Article  CAS  PubMed  Google Scholar 

  • Symondson WOC, Liddell JE (1995) Decay rates for slug antigens within the carabid predator Pterostichus melanarius monitored with a monoclonal antibody. Entomol Exp Appl 75:245–250

    Article  Google Scholar 

  • van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen HMT, Kuske S, Loomans AJM, Menzler-Hokkanen I, van Rijn PCJ, Thomas MB (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38

    Article  Google Scholar 

  • Ware RL, Majerus MEN (2008) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl 53(1):169–188

    Article  Google Scholar 

  • Weber DC, Lundgren JG (2009a) Assessing the trophic ecology of the Coccinellidae: their roles as predators and as prey. Biol Control 51:199–214

    Article  Google Scholar 

  • Weber DC, Lundgren JG (2009b) Detection of predation using qPCR: Effect of prey quantity, elapsed time, chaser diet, and sample preservation on detectable quantity of prey DNA. J Insect Sci 41:1–12

    Article  Google Scholar 

  • Wilcove DS, Rothstein D, Dubow J, Phillips E, Lobos E (1998) Quantifying threats to imperilled species in the United States. Bioscience 48:607–615

    Article  Google Scholar 

  • Yasuda H, Shinya Y (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42:153–163

    Article  Google Scholar 

  • Zaidi RH, Jaal Z, Hawkes NJ, Hemingway J, Symondson WOC (1999) Can multiple-copy sequences of prey DNA be detected amongst the gut contents of invertebrate predators? Mol Ecol 8:2081–2087

    Article  CAS  PubMed  Google Scholar 

  • Zhang GF, Lü ZC, Wan FH (2007) Detection of Bemisia tabaci remains in predator guts using a sequence-characterised amplified region marker. Entomol Exp Appl 123:81–90

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Thibaut Olivier, Laurent Grumiau, Olivier Pigeon and James Harwood for their help in the estimation of the costs and time required for some of the techniques discussed, Manja Künzli, Mario Waldburger, Jamie Trotman, Benedict Odii and Styliana Phillipou for their contribution to the development of feeding experiments and three anonymous reviewers for their help in improving the manuscript.

Author information

Authors and Affiliations

  1. Agroscope Reckenholz-Tänikon, Research Station ART, Reckenholzstrasse 191, 8046, Zürich, Switzerland

    Alexandre Aebi & Renate Zindel

  2. Animal and Environment Research Group, Department of Life Sciences, Anglia Ruskin University, East Road, Cambridge, CB1 1PT, UK

    Peter M. J. Brown & Alison Thomas

  3. Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000, Ghent, Belgium

    Patrick De Clercq & Brecht Ingels

  4. Centre wallon de Recherches agronomiques, Département Sciences du vivant, Unité Protection des plantes et écotoxicologie, Rue de Liroux, 2, 5030, Gembloux, Belgium

    Louis Hautier

  5. Université Libre de Bruxelles, Lutte biologique et Ecologie spatiale, CP 160/12, Av. F.D. Roosevelt 50, 1050, Bruxelles, Belgium

    Louis Hautier

  6. Forest & Landscape, Faculty of Life Sciences, University of Copenhagen, Rolighedsvej 23, 1958, Frederiksberg, Denmark

    Andy Howe & Hans-Peter Ravn

  7. Kronenburgwerf 58, 4812 XR, Breda, The Netherlands

    John J. Sloggett

Authors
  1. Alexandre Aebi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter M. J. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patrick De Clercq
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Louis Hautier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andy Howe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Brecht Ingels
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hans-Peter Ravn
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. John J. Sloggett
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Renate Zindel
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Alison Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexandre Aebi.

Additional information

Handling Editor: Helen Roy

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aebi, A., Brown, P.M.J., De Clercq, P. et al. Detecting arthropod intraguild predation in the field. BioControl 56, 429–440 (2011). https://doi.org/10.1007/s10526-011-9378-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-011-9378-2

Keywords

Search

Navigation