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A simple and cost-effective molecular method to track predation on Drosophila suzukii in the field

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Abstract

The vinegar fly Drosophila suzukii (Matsumura) is an invasive species that attacks ripening fruits and berries, leading to considerable losses in fruit production. So far, management mainly relies on chemical and cultural control, but additional measures such as biological control are needed. Hence, for the development of sustainable control measures of this pest it is important to identify potential natural enemies such as generalist predators that feed on D. suzukii. Here, we established a simple and cost-effective assay to specifically detect D. suzukii DNA in the guts of arthropod predators. Furthermore, we developed a general Drosophila spp. primer pair to identify predators of Drosophila species in general that might also feed on D. suzukii and to compare predation rates on D. suzukii to those of other Drosophila species. We applied the assays to field-collected predators and identified three predator taxa—earwigs, spiders and predatory bugs—that had fed on D. suzukii. The assays provide a first step towards unravelling the predator community attacking D. suzukii that should be considered as biological control agents but also as non-targets potentially affected by other measures to control this invasive pest.

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References

  • Arnó J, Riudavets J, Gabarra R (2012) Survey of host plants and natural enemies of Drosophila suzukii in an area of strawberry production in Catalonia (northeast Spain). IOBC-WPRS Bull 80:29–34

    Google Scholar 

  • Asplen MK, Anfora G, Biondi A, Choi DS, Chu D et al (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494

    Article  Google Scholar 

  • Bächli G (1998) Drosophilidae. In: Merz B, Bächli G, Haenni J-P, Gonsetz Y (eds) Diptera—Checklist. Fauna Helvetica 1. Schweizerische Entomologische Gesellschaft, pp 304–305

  • Bächli G, Burla H (1985) Insecta Helvetica Bd. 7: Diptera – Drosophilidae. Schweizerische Entomologische Gesellschaft

  • Baroffio C, Huber B, Kopp M et al (2016) Drosophila suzukii—Strategie 2016 für die Beerenkulturen. Merkblatt Nr. 38. Ed., Agroscope, Switzerland

  • Canty A, Ripley B (2016) boot: Bootstrap R (S-Plus) Functions. R package version 1.3-18

  • Chabert S, Allemand R, Poyet M, Eslin P, Gibert P (2012) Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biol Control 63:40–47

    Article  Google Scholar 

  • Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull Insectol 65:149–160

    Google Scholar 

  • Core Team R (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Cuthbertson AGS, Blackburn LF, Audsley N (2014) Efficacy of commercially available invertebrate predators against Drosophila suzukii. Insects 5:952–960

    Article  PubMed  PubMed Central  Google Scholar 

  • Daane KM, Wang X-G, Biondi A, Miller B, Miller JC et al (2016) First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci 89:823–835

    Article  Google Scholar 

  • Dhami MK, Kumarasinghe L (2014) A HRM real-time PCR assay for rapid and specific identification of the emerging pest spotted-wing Drosophila (Drosophila suzukii). PLoS ONE 9:e98934

    Article  PubMed  PubMed Central  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. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Frank SD, Wratten SD, Sandhu HS, Shrewsbury PM (2007) Video analysis to determine how habitat strata affects predator diversity and predation of Epiphyas postvittana (Lepidoptera: tortricidae) in a vineyard. Biol Control 41:230–236

    Article  Google Scholar 

  • Gabarra R, Riudavets J, Rodríguez GA, Pujade-Villar J, Arnó J (2015) Prospects for the biological control of Drosophila suzukii. Biocontrol 60:331–339

    Article  Google Scholar 

  • Geiger F, Wäckers FL, Bianchi FJJA (2009) Hibernation of predatory arthropods in semi-natural habitats. Biocontrol 54:529–535

    Article  Google Scholar 

  • Greenstone MH, Weber DC, Coudron TA, Payton ME, Hu JS (2012) Removing external DNA contamination from arthropod predators destined for molecular gut-content analysis. Mol Ecol Resour 12:464–469

    Article  PubMed  Google Scholar 

  • Greenstone MH, Payton ME, Weber DC, Simmons AM (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

    Article  PubMed  Google Scholar 

  • Gurr GM, Wratten SD, Landis DA, You M (2017) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62:91–109

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hamby KA, Bellamy DE, Chiu JC, Lee JC, Walton VM et al (2016) Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. J Pest Sci 89:605–619

    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 

  • Haye T, Girod P, Cuthbertson AGS, Wang XG, Daane KM et al (2016) Current SWD IPM tactics and their practical implementation in fruit crops across different regions around the world. J Pest Sci 89:643–651

    Article  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    Article  CAS  Google Scholar 

  • Höhn H, Lahusen A, Eder R, Ackermann T, Franck L et al (2007) Régulation du psylle du poirier: résultats et observations de 2002 à 2006 en Suisse alémanique. Revue suisse Vitic Arboric Hortic 39:169–176

    Google Scholar 

  • Kenis M, Tonina L, Eschen R, van der Sluis B, Sancassani M et al (2016) Non-crop plants used as hosts by Drosophila suzukii in Europe. J Pest Sci 89:735–748

    Article  Google Scholar 

  • Kim SHS, Tripodi AD, Johnson DT, Szalanski AL (2014) Molecular diagnostics of Drosophila suzukii (Diptera: Drosophilidae) using PCR-RFLP. J Econ Entomol 107:1292–1294

    Article  CAS  PubMed  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 

  • Knoll V, Ellenbroek T, Romeis J, Collatz J (2017) Seasonal and regional presence of hymenopteran parasitoids of Drosophila in Switzerland and their ability to parasitize the invasive Drosophila suzukii. Sci Rep 7:40697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JC, Dreves AJ, Cave AM, Kawai S, Isaacs R et al (2015) Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Ann Entomol Soc Am 108:117–129

    Article  Google Scholar 

  • Lo Giudice G, Woźnica AJ (2013) An updated checklist of the Italian Heleomyzidae (Diptera: Sphaeroceroidea). Genus 24:439–458

    Google Scholar 

  • Long EO, Dawis IB (1980) Repeated genes in eukaryotes. Ann Rev Biochem 49:727–764

    Article  CAS  PubMed  Google Scholar 

  • Malagnini V, Zanotelli L, Tolotti G, Profaizer D, Ahgeli G (2014) Evaluation of predatory activity of Orius laevigatus (Fieber) and O. maiusculus Reuter towards Drosophila suzukii (Matsumura) under laboratory conditions. IOBC/WPRS Working Group “Integrated Protection of Fruit Crops”. In: VIII Workshop on Integrated Soft Fruit Production, Vigalzano di Pergine Valsugana (TN), 26–28 May 2014. Book of Apstracts p 122. http://www.scienzaegoverno.org/sites/default/files/file_attach/Abstract%20Congresso%20IOBC.pdf.pdf

  • Mansfield S, Hagler JR (2016) Wanted dead or alive: scavenging versus predation by three insect predators. Food Webs 9:12–17

    Article  Google Scholar 

  • Mazzetto F, Marchetti E, Amiresmaeili N, Sacco D, Francati S et al (2016) Drosophila parasitoids in northern Italy and their potential to attack the exotic pest Drosophila suzukii. J Pest Sci 89:837–850

    Article  Google Scholar 

  • Mazzi D, Bravin E, Meraner M, Finger R, Kuske S (2017) Economic impact of the introduction and establishment of Drosophila suzukii on sweet cherry production in Switzerland. Insects 8:18

    Article  PubMed Central  Google Scholar 

  • Michalko R, Pekár S (2016) Different hunting strategies of generalist predators result in functional differences. Oecologia 181:1187–1197

    Article  PubMed  Google Scholar 

  • Monzó C, Sabater-Muñoz B, Urbaneja A, Castañera P (2011) The ground beetle Pseudophonus rufipes revealed as predator of Ceratitis capitata in citrus orchards. Biol Control 56:17–21

    Article  Google Scholar 

  • Moser SE, Kajita Y, Harwood JD, Obrycki JJ (2011) Evidence for utilization of Diptera in the diet of field-collected coccinellid larvae from an antibody-based detection system. Biol Control 58:248–254

    Article  Google Scholar 

  • Murphy KA, Unruh TR, Zhou LM, Zalom FG, Shearer PW et al (2015) Using comparative genomics to develop a molecular diagnostic for the identification of an emerging pest Drosophila suzukii. Bull Entomol Res 105:364–372

    Article  CAS  PubMed  Google Scholar 

  • Nicholas AH, Spooner-Hart RN, Vickers RA (2005) Abundance and natural control of the woolly aphid Eriosoma lanigerum in an Australian apple orchard IPM program. Biocontrol 50:271–291

    Article  Google Scholar 

  • Nyffeler M (1999) Prey selection of spiders in the field. J Arachnol 27:317–324

    Google Scholar 

  • Payton ME, Greenstone MH, Schenker N (2003) Overlapping confidence intervals or standard error intervals: What do they mean in terms of statistical significance? J Insect Sci 3:34

    Article  PubMed  PubMed Central  Google Scholar 

  • Poyet M, Le Roux V, Gibert P, Meirland A, Prévost G et al (2015) The wide potential trophic niche of the Asiatic fruit fly Drosophila suzukii: the key of its invasion success in temperate Europe? PLoS ONE 10:e0142785

    Article  PubMed  PubMed Central  Google Scholar 

  • Renkema JM, Telfer Z, Gariepy T, Hallett RH (2015) Dalotia coriaria as a predator of Drosophila suzukii: functional responses, reduced fruit infestation and molecular diagnostics. Biol Control 89:1–10

    Article  CAS  Google Scholar 

  • Romeu-Dalmau C, Piñol J, Agustí N (2012a) Detecting aphid predation by earwigs in organic citrus orchards using molecular markers. Bull Entomol Res 102:566–572

    Article  CAS  PubMed  Google Scholar 

  • Romeu-Dalmau C, Piñol J, Espadaler X (2012b) Friend or foe? The role of earwigs in a Mediterranean organic citrus orchard. Biol Control 63:143–149

    Article  Google Scholar 

  • Roubos CR, Rodriguez-Saona C, Holdcraft R, Mason KS, Isaacs R (2014) Relative toxicity and residual activity of insecticides used in blueberry pest management: mortality of natural enemies. J Econ Entomol 107:277–285

    Article  PubMed  Google Scholar 

  • Sint D, Raso L, Traugott M (2012) Advances in multiplex PCR: balancing primer efficiencies and improving detection success. Methods Ecol Evol 3:898–905

    Article  PubMed  PubMed Central  Google Scholar 

  • Sint D, Niederklapfer B, Kaufmann R, Traugott M (2014) Group-specific multiplex PCR detection systems for the identification of flying insect prey. PLoS ONE 9:e115501

    Article  PubMed  PubMed Central  Google Scholar 

  • Soszyńska-Maj K, Woźnica AJ (2016) A case study of Heleomyzidae (Diptera) recorded on snow in Poland with a review of their winter activity in Europe. Eur J Entomol 113:279–294

    Article  Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    Article  CAS  PubMed  Google Scholar 

  • Tourmente S, Lecher P, Degroote F, Renaud M (1990) Mitochondrial development during Drosophila oogenesis: distribution, density and in situ RNA hybridizations. Biol Cell 68:119–127

    Article  CAS  PubMed  Google Scholar 

  • Traugott M, Kamenova S, Ruess L, Seeber J, Plantegenest M (2013) Empirically characterising trophic networks: what emerging DNA-based methods, stable isotope and fatty acid analyses can offer. Adv Ecol Res 49:177–224

    Article  Google Scholar 

  • Tschumi M, Albrecht M, Collatz J, Dubsky V, Entling MH et al (2016) Tailored flower strips promote natural enemy biodiversity and pest control in potato crops. J Appl Ecol 53:1169–1176

    Article  Google Scholar 

  • Unruh TR, Miliczky ER, Horton DR, Thomsen-Archer K, Rehfield-Ray L et al (2016) Gut content analysis of arthropod predators of codling moth in Washington apple orchards. Biol Control 102:85–92

    Article  Google Scholar 

  • Urbaneja A, García Marí F, Tortosa D, Navarro C, Vanaclocha P et al (2006) Influence of ground predators on the survival of the Mediterranean fruit fly pupae, Ceratitis capitata, in Spanish citrus orchards. Biocontrol 51:611–626

    Article  Google Scholar 

  • Van Zuijlen JWA, Roháček J (2009) Opomyzidae. In: Roháček J, Ševčík J (eds) Diptera of the Pol’ana Protected Landscape Area—Biosphere Reserve (Central Slovakia). SNC SR, Administration of the PLA—BR Pol’ana, Zvolen, pp 236–237

  • Wallinger C, Staudacher K, Schallhart N, Peter E, Dresch P et al (2013) The effect of plant identity and the level of plant decay on molecular gut content analysis in a herbivorous soil insect. Mol Ecol 13:75–83

    Article  CAS  Google Scholar 

  • Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee J et al (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:G1–G7

    Article  Google Scholar 

  • Wang X-G, Stewart TJ, Biondi A, Chavez BA, Ingels C et al (2016) Population dynamics and ecology of Drosophila suzukii in Central California. J Pest Sci 89:701–712

    Article  Google Scholar 

  • Woltz JM, Lee JC (2017) Pupation behaviour and larval and pupal biocontrol of Drosophila suzukii in the field. Biol Control 110:62–69

    Article  Google Scholar 

  • Woltz JM, Donahue KM, Bruck DJ, Lee JC (2015) Efficacy of commercially available predators, nematodes and fungal entomopathogens for augmentative control of Drosophila suzukii. J Appl Entomol 139:759–770

    Article  Google Scholar 

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Acknowledgements

This work was funded by the Drosophila suzukii R & D Task Force funded by the Swiss Federal Office for Agriculture (FOAG). Additional support for molecular analysis by Agroscope is gratefully acknowledged. The authors thank Gerhard Bächli for providing specimens of drosophilids and for his assistance in identifying Drosophila species. We are grateful to Serge Fischer (Agroscope), Pierre Girod (CABI), Steffen Hagenbucher (Wildbiene und Partner) and Florian Steiner (University of Innsbruck) for providing specimens of Drosophila species. We thank Alexander Rief (University of Innsbruck) for his assistance in identifying spiders. We also thank Sara D’Alessio and Daniel Hauser (Agroscope) for their help in the field survey. Moreover, many thanks go to the farmers and neighbours that allowed us to collect predators in their cultures. We also want to thank the three anonymous reviewers for their valuable comments that helped improve the manuscript.

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Authors and Affiliations

  1. Agroscope, Research Division Agroecology and Environment, Reckenholzstrasse 191, 8046, Zurich, Switzerland

    Sarah Wolf, Jörg Romeis & Jana Collatz

  2. Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Technikerstrasse 25, 6020, Innsbruck, Austria

    Christiane Zeisler, Daniela Sint & Michael Traugott

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  1. Sarah Wolf
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  2. Christiane Zeisler
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Correspondence to Jana Collatz.

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Communicated by A. Biondi.

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Wolf, S., Zeisler, C., Sint, D. et al. A simple and cost-effective molecular method to track predation on Drosophila suzukii in the field. J Pest Sci 91, 927–935 (2018). https://doi.org/10.1007/s10340-017-0948-7

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