Eur. J. Entomol. 118: 335-343, 2021 | DOI: 10.14411/eje.2021.035

PCR-based detection of prey DNA in the gut contents of the tiger-fly, Coenosia attenuata (Diptera: Muscidae), a biological control agent in Mediterranean greenhousesOriginal article

Sofia G. SEABRA ORCID...1, Joana MARTINS2, Patrícia BRÁS1, Ana M. TAVARES1, Inês FREITAS1, António BARATA1, Maria Teresa REBELO ORCID...3, Célia MATEUS4, Octávio S. PAULO ORCID...1, Elisabete FIGUEIREDO ORCID...2
1 Centre for Ecology, Evolution and Environmental Changes (cE3c), Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal; e-mails: sgseabra@gmail.com, patricia.g.bras@gmail.com, anamptavares@gmail.com, ifinesfreitas@hotmail.com, apbarata@gmail.com, octavio.paulo@fc.ul.pt
2 Linking Landscape, Environment, Agriculture and Food (LEAF), Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal; e-mails: joanar.fmartins@gmail.com, elisalacerda@isa.ulisboa.pt
3 Centre for Environmental and Marine Studies (CESAM), Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal; e-mail: mtrebelo@fc.ul.pt
4 Instituto Nacional de Investigação Agrária e Veterinária (INIAV), Av. da República, Quinta do Marquês, 2780-157 Oeiras, Portugal; e-mail: celia.mateus@iniav.pt

The tiger-fly Coenosia attenuata Stein (Diptera: Muscidae: Coenosiini) is a generalist predator that preys on several pests of greenhouse crops and is considered a biological control agent in the Mediterranean region. Previous behavioural observations identified its preferred prey, but a more in-depth evaluation will benefit from using Polymerase Chain Reaction amplification of prey DNA remains in the gut of this predator. To evaluate the rate of decay and suitability of this method for use in the field assessments, we carried out a laboratory feeding calibration experiment on 355 females of C. attenuata, which were killed at different intervals of time after ingestion (10 time points from 0 to 48 h). The prey species tested were: Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae: Trialeurodini), Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae), Diglyphus isaea (Walker) (Hymenoptera: Eulophidae: Cirrospilini), Bradysia impatiens (Johannsen) (Diptera: Sciaridae) and Drosophila mercatorum Patterson & Wheeler (Diptera: Drosophilidae: Drosophilini). Based on a probit model, amplification success of prey DNA declined exponentially with increasing time after ingestion. The half-time molecular detection differed between species, ranging from an average of 5 h for T. vaporariorum and D. isaea, 6 h for B. impatiens, 15 h for L. huidobrensis to more than 40 h for D. mercatorum. This study confirmed the feasibility of using DNA based detection to identify prey species in the gut contents of C. attenuata and provided calibration curves for a better understanding of predation activity in this agroecosystem.

Keywords: Diptera, Muscidae, Coenosia attenuata, predation, gut contents, prey molecular identification, Polymerase Chain Reaction, probit models, half-time molecular detection

Received: February 20, 2021; Revised: September 24, 2021; Accepted: September 24, 2021; Published online: October 28, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
SEABRA, S.G., MARTINS, J., BRÁS, P., TAVARES, A.M., FREITAS, I., BARATA, A., ... FIGUEIREDO, E. (2021). PCR-based detection of prey DNA in the gut contents of the tiger-fly, Coenosia attenuata (Diptera: Muscidae), a biological control agent in Mediterranean greenhouses. EJE, 118, Article 335-343. https://doi.org/10.14411/eje.2021.035
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Bautista-Martínez N., Illescas-Riquelme C.P. & García-Ávila C.J. 2017: First report of "hunter-fly" Coenosia attenuata (Diptera: Muscidae) in Mexico. - Fla Entomol. 100: 174-175. Go to original source...
    2. Chen Y., Giles K.L., Payton M.E. & Greenstone M.H. 2000: Identifying key cereal aphid predators by molecular gut analysis. - Mol. Ecol. 9: 1887-1898. Go to original source...
    3. Figueiredo E., Mexia A., Mateus C., Godinho M. & Rodrigues S. 2011: Integrated pest management in vegetable protected crops in the Oeste region. - Acta Hortic. 917: 93-101. Go to original source...
    4. Figueiredo E., Martins J., Nunes R., Garcia A., Franco J.C. & Mateus C. 2016: The tiger-fly Coenosia attenuata as a potential biological control agent in vegetable protected crops. In Gerling D., Steinberg S. & Coll M. (eds): Proceedings of the 9th Meeting "Pest Management in an Ever-Changing World" at the Robert H. Smith Faculty of Agriculture, Food & Environment, The Hebrew University of Jerusalem, Rehovot (Israel), October 11-15, 2015. - IOBC-WPRS Bull. 119: 32-33.
    5. 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. - Mol. Ecol. 14: 4147-4158. Go to original source...
    6. Gagnon A.E.Á., Doyon J., Heimpel G.E. & Brodeur J. 2011: Prey DNA detection success following digestion by intraguild predators: influence of prey and predator species. - Mol. Ecol. Resour. 11: 1022-1032. Go to original source...
    7. Gilioli G., Baumgartner J. & Vacante V. 2005: Temperature influences on functional response of Coenosia attenuata (Diptera: Muscidae) individuals. - J. Econ. Entomol. 98: 1524-1530. Go to original source...
    8. 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. - Bull. Entomol. Res. 97: 201-209. Go to original source...
    9. Greenstone M.H., Payton M.E., Weber D.C. & Simmons A.M. 2014: The detectability half-life in arthropod predator-prey research: what it is, why we need it, how to measure it, and how to use it. - Mol. Ecol. 23: 3799-3813. Go to original source...
    10. 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. - Biol. Contr. 9: 112-119. Go to original source...
    11. Hajibabaei M., Janzen D.H., Burns J.M., Hallwachs W. & Hebert P.D.N. 2006: DNA barcodes distinguish species of tropical Lepidoptera. - Proc. Nat. Acad. Sci. USA 103: 968-971. Go to original source...
    12. 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...
    13. Hebert P.D.N., Cywinska A., Ball S.L. & deWaard J.R. 2003: Biological identifications through DNA barcodes. - Proc. R. Soc. (B) 270: 313-321. Go to original source...
    14. Hennig W. 1964: Muscidae: Gattung Coenosia Meigen, section 63b. In Lindner E. (ed.): 7: Die Fliegen der Palaearktischen Region. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart, pp. 518-619.
    15. 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. - Mol. Ecol. 10: 2059-2067. Go to original source...
    16. Howarth F.G. 2000: Non-target effects of biological control agents. In Gurr G. & Wratten S. (eds): Biological Control: Measures of Success. Springer, Dordrecht, pp. 369-403. Go to original source...
    17. Jarman S.N. 2004: Amplicon: software for designing PCR primers on aligned DNA sequences. - Bioinformatics 20: 1644-1645. Go to original source...
    18. King R. 2008: Molecular analysis of predation: a review of best practice for DNA-based approaches. - Mol. Ecol. 17: 947-963. Go to original source...
    19. King R.A., Moreno-Ripoll R., Agustí N., Shayler S.P., Bell J.R., Bohan D.A. & Symondson W.O.C. 2011: Multiplex reactions for the molecular detection of predation on pest and nonpest invertebrates in agroecosystems. - Mol. Ecol. Resour. 11: 370-373. Go to original source...
    20. Kühne S. 1998: Open rearing of generalist predators: a strategy for improvement of biological pest control in greenhouses. - Phytoparasitica 26: 277-281. Go to original source...
    21. Kühne S. 2000: Räuberische Fliegen der Gattung Coenosia Meigen, 1826 (Diptera: Muscidae) und die Möglichkeit ihres Einsatzes bei der biologischen Schädlingsbekämpfung. - Stud. Dipterol. (Suppl.) 9: 1-78.
    22. LeOra Software 1987: POLO-PC: A Users Guide to Probit or Logit Analysis. LeOra Software, Berkeley.
    23. Louda S.M., Pemberton R.W., Johnson M.T. & Follett P.A. 2003: Nontarget effects - The Achilles' heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. - Annu. Rev. Entomol. 48: 365-396. Go to original source...
    24. 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). - J. Entomol. Nematol. 129: 330-335. Go to original source...
    25. Macías-Hernández N., Athey K., Tonzo V., Wangensteen O.S., Arnedo M. & Harwood J.D. 2018: Molecular gut content analysis of different spider body parts. - PLoS ONE 13(5): e0196589, 16 pp. Go to original source...
    26. Martinez M. & Cocquempot C. 2000: La mouche Coenosia attenuata, un nouvel auxiliaire prometteur en culture protégée. - PHM Rev. Hort. 414: 50-52.
    27. Martins J., Domingos C., Nunes R., Garcia A., Ramos C., Mateus C. & Figueiredo E. 2012: Coenosia attenuata (Diptera: Muscidae), um predador em estudo para utilização em culturas protegidas. - Revta Ciênc. Agrár. 35: 229-235.
    28. Martins J., Mateus C., Ramos A.C. & Figueiredo E. 2015: An optimized method for mass rearing the tiger-fly, Coenosia attenuata (Diptera: Muscidae). - Eur. J. Entomol. 112: 470-476. Go to original source...
    29. Mateus C. 2012: Bioecology and behaviour of Coenosia attenuata in greenhouse vegetable crops in the Oeste region, Portugal. - Bull. Insectol. 65: 257-263.
    30. Moreschi I. & Süss L. 1998: Osservazioni biologiche ed etologische su Coenosia attenuata Stein e Coenosia strigipes Stein (Diptera: Muscidae). - Boll. Zool. Agrar. Bachicolt. 30: 185-197.
    31. Morris D.E. & Cloutier C. 1987: Biology of the predatory fly Coenosia tigrina (Fab.) (Diptera: Anthomyiidae): reproduction, development, and larval feeding on earthworms in the laboratory. - Can. Entomol. 119: 381-393. Go to original source...
    32. Paula D.P., Linard B., Crampton-Platt A., Srivathsan A., Timmermans M.J.T.N., Sujii E.R., Pires C.S.S., Souza L.M., Andow D.A. & Vogler A.P. 2016: Uncovering trophic interactions in arthropod predators through DNA shotgun-sequencing of gut contents. - PLoS ONE 11(9): e0161841, 14 pp. Go to original source...
    33. Pohl D., Kühne S., Karaca I. & Moll E. 2012: Review of Coenosia attenuata Stein and its first record as a predator of important greenhouse pests in Turkey. - Phytoparasitica 40: 63-68. Go to original source...
    34. Pompanon F., Deagle B.E., Symondson W.O.C., Brown D.S., Jarman S.N. & Taberlet P. 2012: Who is eating what: diet assessment using next generation sequencing. - Mol. Ecol. 21: 1931-1950. Go to original source...
    35. Prieto R., Figueiredo E. & Mexia A. 2005: Coenosia attenuata Stein (Diptera: Muscidae): prospecção e actividade em culturas protegidas em Portugal. - Bol. Sanid. Veget. Plagas 31: 39-45.
    36. Robertson J.L., Jones M.M., Olguin E. & Alberts B. 2017: Bioassays with Arthropods. 3rd ed. CRC Press, Taylor & Francis Group, Boca Raton, 212 pp. Go to original source...
    37. Seabra S.G., Brás P.G., Martins J., Martins R., Wyatt N., Shirazi J., Rebelo M.T., Franco J.C., Mateus C., Figueiredo E. & Paulo O.S. 2015: Phylogeographic patterns in Coenosia attenuata (Diptera: Muscidae), a widespread predator of insect species associated with greenhouse crops. - Biol. J. Linn. Soc. 114: 308-326. Go to original source...
    38. Sheppard S.K. & Harwood J.D. 2005: Advances in molecular ecology: tracking trophic links through predator - prey food-webs. - Funct. Ecol. 19: 751-762. Go to original source...
    39. Stilin P. & Simberloff D. 2000: The frequency and strength of nontarget effects of invertebrate biological control agents of plant pests and weeds. In Follett P.A. & Duan J.J. (eds): Nontarget Effects of Biological Control. Springer Science + Business Media, New York, pp. 31-44. Go to original source...
    40. Symondson W.O.C., Sunderland K.D. & Greenstone M.H. 2002: Can generalist predators be effective biocontrol agents? - Annu. Rev. Entomol. 47: 561-594. Go to original source...
    41. Tellez M.D.M., Tapia G., Gamez M., Cabello T. & Vanemden H. 2009: Predation of Bradysia sp. (Diptera: Sciaridae), Liriomyza trifolii (Diptera: Agromyzidae) and Bemisia tabaci (Hemiptera: Aleyrodidae) by Coenosia attenuata (Diptera: Muscidae) in greenhouse crops. - Eur. J. Entomol. 106: 199-204. 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.


    Return to the content