Skip to main content
SpringerLink
Log in

An invader supported by a parasite: Mistletoe berries as a host for food and reproduction of Spotted Wing Drosophila in early spring

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

The Spotted Wing Drosophila (SWD), Drosophila suzukii Matsumura, an invasive pest species in Europe and the Americas, is able to feed and reproduce on numerous fruit crops and a wide range of wild host plants. SWD is thought to overwinter outside of agricultural fields in forests and hedges. To identify overwintering sites and early spring oviposition hosts, traps were installed in forests. In spring 2015, traps in the canopy of pine trees parasitized by mistletoe, Viscum album subsp. laxum, captured significantly more SWD than traps in pine trees without mistletoe. We found SWD females with ripe eggs coinciding with ripening and ripe mistletoe berries. We investigated whether mistletoe may serve as a host for SWD. Under laboratory conditions, SWD developed from egg to adult in mistletoe berries. More adults emerged from wounded berries. Females were observed to feed on berries and survived up to eight days without other food. A few adults emerged from wild mistletoe berries. To understand the attraction of SWD to parasitized trees, we analyzed the volatile organic compounds (VOCs) collected from the headspace of mistletoe berries by GC–MS and identified the main components. Thirty-two VOCs were found. Wounded and unwounded berries differed significantly in the quantity of 11 VOCs emitted. The odor spectrum showed many similarities to other typical berry odors. The combination of field surveys and laboratory assays identified a new reproduction host for SWD in spring. This host plant may help SWD to withstand the bottleneck period for survival in winter and spring.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abraham J, Zhang A, Angeli S, Abubeker S, Michel C, Feng Y, Rodriguez-Saona C (2015) Behavioral and antennal responses of Drosophila suzukii (Diptera: Drosophilidae) to volatiles from fruit extracts. Environ Entomol 44:356–367. doi:10.1093/ee/nvv013

    Article  PubMed  Google Scholar 

  • Asplen MK, Anfora G, Biondi A, Choi DS, Chu D, Daane KM, Gibert P, Gutierrez AP, Hoelmer KA, Hutchison WD, Isaacs R, Jiang ZL, Karpati Z, Kimura MT, Pascual M, Philips CR, Plantamp C, Ponti L, Vetek G, Vogt H, Walton VM, Yu Y, Zappala L, Desneux N (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494. doi:10.1007/s10340-015-0681-z

    Article  Google Scholar 

  • Bellamy DE, Sisterson MS, Walse SS (2013) Quantifying host potentials: indexing postharvest fresh fruits for spotted wing Drosophila, Drosophila suzukii. PLoS One 8:e61227. doi:10.1371/journal.pone.0061227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breunig T, Demuth S (2000) Naturführer Mannheim: Entdeckungen im Quadranten. Stadt Mannheim u. Bezirksstelle für Naturschutz und Landschaftspflege Karlsruhe (Hrsg.) - 132 S.; Verlag regionalkultur, Ubstadt-Weiher

  • Briem F, Breuer M, Kirsten K, Vogt H (2015) Phenology and occurrence of spotted wing Drosophila in Germany and case studies for its control in berry crops. IOBC-WPRS Bull 109:233–237

    Google Scholar 

  • Bungert M, Thiel R, Goedings P, Becker H (2002) (E, E)-alpha-farnesene the main substance of the volatiles of the flowers from European mistletoe (Viscum album L.). Z Naturforsch C 57:205–207

    Article  CAS  PubMed  Google Scholar 

  • Calabria G, Maca J, Bachli G, Serra L, Pascual M (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147. doi:10.1111/j.1439-0418.2010.01583

    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 

  • Cini A, Anfora G, Escudero-Colomar LA, Grassi A, Santosuosso U, Seljak G, Papini A (2014) Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. J Pest Sci 87:559–566. doi:10.1007/s10340-014-0617-z

    Article  Google Scholar 

  • Crawley MJ (2002) Statistical computing. An introduction to data analysis using S-Plus. Wiley, New York

    Google Scholar 

  • Dalton DT, Walton VM, Shearer PW, Walsh DB, Caprile J, Isaacs R (2011) Laboratory survival of Drosophila suzukii under simulated winter conditions of the Pacific Northwest and seasonal field trapping in five primary regions of small and stone fruit production in the United States. Pest Manag Sci 67:1368–1374. doi:10.1002/ps.2280

    Article  CAS  PubMed  Google Scholar 

  • Deprá M, Poppe JL, Schmitz HJ, De Toni DC, Valente VLS (2014) The first records of the invasive pest Drosophila suzukii in the South American continent J. Pest Sci 87:379–383. doi:10.1007/s10340-014-0591-5

    Article  Google Scholar 

  • Dicke M, van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324. doi:10.1038/nchembio.169

    Article  CAS  PubMed  Google Scholar 

  • Gerdeman BS, Tanigoshi LK (2012) Comparative reproductive condition between laboratory cultures and field collected Spotted Wing Drosophila in the Pacific Northwest. 8th International Conference on Integrated Fruit Production IOBC wprs, Kusadasi 2012, Abstract Book p. 124

  • Hamby KA, Bolda MP, Sheehan ME, Zalom FG (2014) Seasonal monitoring for Drosophila suzukii (Diptera: Drosophilidae) in California commercial raspberries. Environ Entomol 43:1008–1018. doi:10.1603/EN13245

    Article  CAS  PubMed  Google Scholar 

  • Harris DW, Hamby KA, Wilson HE, Zalom FG (2014) Seasonal monitoring of Drosophila suzukii (Diptera: Drosophilidae) in a mixed fruit production system. J Asia-Pacif Entomol 17:857–864. doi:10.1016/j.aspen.2014.08.006

    Article  Google Scholar 

  • Hauser M (2011) A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag Sci 67:1352–1357. doi:10.1002/ps.2265

    Article  CAS  PubMed  Google Scholar 

  • Heil M (2007) Indirect defence via tritrophic interactions. New Phytol 178:41–61. doi:10.1111/j.1469-8137.2007.02330.x

    Article  PubMed  Google Scholar 

  • Heuck P (2012) Drosophila suzukii erstmals für Deutschland (Diptera: Drosophilidae). NachrBl bayer Ent 61(1/2):46

    Google Scholar 

  • Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800–803. doi:10.1093/biomet/75.4.800

    Article  Google Scholar 

  • Ioriatti C, Walton V, Dalton D, Anfora G, Grassi A, Maistri S, Mazzoni V (2015) Drosophila suzukii (Diptera: Drosophilidae) and its potential impact to wine grapes during harvest in two cool climate wine grape production regions. J Econ Entomol 108:1148–1155. doi:10.1093/jee/tov042

    Article  CAS  PubMed  Google Scholar 

  • Jakobs R, Gariepy TD, Sinclair BJ (2015) Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii. J Insect Physiol 79:1–9. doi:10.1016/j.jinsphys.2015.05.003

    Article  CAS  PubMed  Google Scholar 

  • Keesey IW, Knaden M, Hansson BS (2015) Olfactory specialization in Drosophila suzukii supports an ecological shift in host preference from rotten to fresh fruit. J Chem Ecol 41:121–128. doi:10.1007/s10886-015-0544-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • King RC, Rubinson AC, Smith RF (1956) Oogenesis in adult Drosophila melanogaster. Growth 20:121–157

    CAS  PubMed  Google Scholar 

  • Knudsen JT, Tollsten L, Bergström LG (1993) Floral scents—a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253–280

    Article  CAS  Google Scholar 

  • Köppler K, Vogt H (2015) Versuchsergebnisse zusammengetragen und Vorgehen für 2015 abgestimmt—3. Treffen der Arbeitsgruppe Kirschessigfliege: Wertvolle Zusammenarbeit über die Landesgrenzen hinweg. Obstbau 5:318–320

    Google Scholar 

  • Lee JC, Bruck DJ, Dreves AJ, Ioriatti C, Vogt H, Baufeld P (2011) In focus: spotted wing drosophila, Drosophila suzukii, across perspectives. Pest Manag Sci 67:1349–1351. doi:10.1002/ps.2271

    Article  CAS  PubMed  Google Scholar 

  • Lee JC, Dreves AJ, Cave AM, Kawai S, Isaacs R, Miller JC, Van Timmeren S, Bruck DJ (2015) Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Ann Entomol Soc Am 108:117–129. doi:10.1093/aesa/sau014

    Article  Google Scholar 

  • Lenth R (2015) lsmeans: least-squares means. R package version 2.21-1. http://CRAN.R-project.org/package=lsmeans

  • Mann RS, Ali JG, Hermann SL, Tiwari S, Pelz-Stelinski KS, Alborn HT, Stelinski LL (2012) Induced release of a plant-defense volatile ‘deceptively’ attracts insect vectors to plants infected with a bacterial pathogen. PLoS Pathog 8:e1002610. doi:10.1371/journal.ppat.1002610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitsui H, Beppu K, Kimura MT (2010) Seasonal life cycles and resource uses of flower- and fruit-feeding drosophilid flies (Diptera: Drosophilidae) in central Japan. Entomol Sci 13:60–67. doi:10.1111/j.1479-8298.2010.00372.x

    Article  Google Scholar 

  • Ometto L, Cestaro A, Ramasamy S, Grassi A, Revadi S, Siozos S, Moretto M, Fontana P, Varotto C, Pisani D, Dekker T, Wrobel N, Viola R, Pertot I, Cavalieri D, Blaxter M, Anfora G, Rota-Stabelli O (2013) Linking Genomics and Ecology to Investigate the Complex Evolution of an Invasive Drosophila Pest. Genome Biol Evol 4:745–757. doi:10.1093/gbe/evt034

    Article  Google Scholar 

  • Pinheiro JC, Bates D (2000) Mixed-effect models in S and S-plus. Springer, New York

    Book  Google Scholar 

  • Pinheiro JC, Bates D, DebRoy S, Sarkar D, and R Core Team (2015) _nlme: linear and nonlinear mixed effects models_. R package version 3.1-122, <URL: http://CRAN.R-project.org/package=nlme>

  • Poyet M, Eslin P, Heraude M, Le Roux V, Prevost G, Gibert P, Chabrerie O (2014) Invasive host for invasive pest: when the Asiatic cherry fly (Drosophila suzukii) meets the American black cherry (Prunus serotina) in Europe. Agric For Entomol 16:251–259. doi:10.1111/afe.12052

    Article  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Revadi S, Vitagliano S, Stacconi MVR, Ramasamy S, Mansourian S, Carlin S, Vrhovsek U, Becher PG, Mazzoni V, Rota-Stabelli O, Angeli S, Dekker T, Anfora G (2015) Olfactory responses of Drosophila suzukii females to host plant volatiles. Physiol Entomol 40:54–64. doi:10.1111/phen.12088

    Article  CAS  Google Scholar 

  • Rid M, Mesca C, Ayasse M, Gross J (2016) Apple proliferation phytoplasma influences the pattern of plant volatiles emitted depending on pathogen virulence. Front Ecol Evol 3:152. doi:10.3389/fevo.2015.00152

    Article  Google Scholar 

  • Steck K, Veit D, Grandy R, Badia SBI, Badia SBI, Mathews Z, Verschure P, Hansson BS, Knaden M (2012) A high-throughput behavioral paradigm for Drosophila olfaction—the flywalk. Sci Rep 2:361. doi:10.1038/srep00361

    Article  PubMed  PubMed Central  Google Scholar 

  • Steffan SA, Lee JC, Singleton ME, Vilaire A, Walsh DB, Lavine LS, Patten K (2013) Susceptibility of Cranberries to Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 106:2424–2427. doi:10.1603/ec13331

    Article  PubMed  Google Scholar 

  • Stephens AR, Asplen MK, Hutchison WD, Venette RC (2015) Cold hardiness of winter-acclimated Drosophila suzukii (Diptera: Drosophilidae) adults. Environ Entomol 44(6):1619–1626. doi:10.1093/ee/nvv134

    Article  CAS  PubMed  Google Scholar 

  • Van Poecke RMP, Posthumus MA, Dicke M (2001) Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol 27:1911–1928. doi:10.1023/A:1012213116515

    Article  PubMed  Google Scholar 

  • Vogt H, Briem F (2015) Die Kirschessigfliege—ein aktueller Überblick. In: 8. Bundesbeerenobstseminar, Weinsberg, Staatliche Lehr- und Versuchsanstalt für Wein- und Obstbau, pp 58–61

  • Vogt H, Hoffmann C, Baufeld P (2012a) Ein neuer Schädling, die Kirschessigfliege, Drosophila suzukii (Matsumura 1931), bedroht Obst- und Weinkulturen. Entomol Nachrichten und Berichte 56:191–196

    Google Scholar 

  • Vogt H, Baufeld P, Gross J, Köppler K, Hoffmann C (2012b) Drosophila suzukii: eine neue Bedrohung für den Europäischen Obst- und Weinbau. Bericht über eine internationale Tagung in Trient, 2. Dezember 2011. J für Kulturpflanzen 64:68–72

    Google Scholar 

  • Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee J, Bruck DJ, Walton VM, O’Neal SD, Zalom FG (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:1–7. doi:10.1603/ipm10010

    Article  Google Scholar 

  • Weintraub PG, Gross J (2013) Capturing insect vectors of phytoplasmas. Methods Mol Biol 938:61–72. doi:10.1007/978-1-62703-089-2_6

    Article  CAS  PubMed  Google Scholar 

  • Wiman NG, Walton VM, Dalton DT, Anfora G, Burrack HJ, Chiu JC, Daane KM, Grassi A, Miller B, Tochen S, Wang X, Ioriatti C (2014) Integrating temperature-dependent life table data into a matrix projection model for Drosophila suzukii population estimation. PLoS One 9:e106909. doi:10.1371/journal.pone.0106909

    Article  PubMed  PubMed Central  Google Scholar 

  • Zerulla F, Schmidt S, Streitberger M, Zebitz C, Zelger R (2015) On the overwintering ability of Drosophila suzukii in South Tyrol. J Berry Res 5:41–48. doi:10.3233/JBR-150089

    Google Scholar 

Download references

Acknowledgments

The authors thank Jürgen Just and Anja Frank (JKI) for technical support in rearing of SWD, monitoring SWD phenology, taking photographs of developmental stages of eggs, and dissection of females. We thank Michael Breuer (State Institute for Viticulture and Enology (WBI), Freiburg, Germany) for briefing us in installing monitoring traps in the canopy of trees. We thank Michael Herwig (forestry commission Mannheim, Germany) for the permit to collect mistletoes in the Dossenwald as well as Peter Burger (JKI) for sampling mistletoes in the meadow orchard near Heddesbach and communicating the contact to the owner family Falter, Heddesbach, Germany. We thank Kai Lukat, Tobias Schneider, Michael Papke (all JKI), and Anna-Maria Baumann (WBI) for assistance in the mistletoe sampling. We thank Svenja Stein and Kai Lukat (JKI) for support in headspace sampling. We are grateful to Doreen Gabriel and Jannicke Gallinger (JKI) for statistical advice. The authors wish to thank Peter Shearer (Oregon State University, USA) for the English revision. Suggestions by three anonymous reviewers greatly improved the manuscript.

Author information

Authors and Affiliations

  1. Laboratory of Entomology, Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Fruit Crops and Viticulture, Julius Kühn-Institut (JKI), Schwabenheimer Straße 101, 69221, Dossenheim, Germany

    Felix Briem, Astrid Eben & Heidrun Vogt

  2. Laboratory of Chemical Ecology, Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Fruit Crops and Viticulture, Julius Kühn-Institut (JKI), Schwabenheimer Straße 101, 69221, Dossenheim, Germany

    Jürgen Gross

Authors
  1. Felix Briem
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Astrid Eben
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jürgen Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Heidrun Vogt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heidrun Vogt.

Additional information

Communicated by A. Biondi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Briem, F., Eben, A., Gross, J. et al. An invader supported by a parasite: Mistletoe berries as a host for food and reproduction of Spotted Wing Drosophila in early spring. J Pest Sci 89, 749–759 (2016). https://doi.org/10.1007/s10340-016-0739-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-016-0739-6

Keywords

Search

Navigation