Skip to main content
Log in

Soil emergence of Drosophila suzukii adults: a susceptible period for entomopathogenic nematodes infection

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

Abstract

Drosophila suzukii is a global invasive pest of soft-skinned and small stone fruits. Fly larvae fall from fruit to the soil to pupate, after which time adults emerge. Biological control of D. suzukii larvae with entomopathogenic nematodes has been reported in previous studies with positive results, but susceptibility of adults has still not been evaluated. In this study, the susceptibility of mature adults to Heterorhabditis bacteriophora, Steinernema feltiae and S. carpocapsae was tested. We also evaluated the infection and dispersion of adults after emerging from soil treated with S. carpocapsae. The results showed that 65% of mature adults were infected with S. carpocapsae while the other nematode treatments barely reached 4% infection. This nematode was also able to reproduce inside the D. suzukii fly. When adults emerged from treated soil, S. carpocapsae infection reached 89%. The results of the dispersion assay showed that 21.4% of nematode-infected adults could fly. These results showed the potential of S. carpocapsae applications to soil in order to control adult emergence of D. suzukii.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arnó J, Solà M, Riudavets J, Gabarra R (2016) Population dynamics, non-crop hosts, and fruit susceptibility of Drosophila suzukii in Northeast Spain. J Pest Sci 89:713–723. https://doi.org/10.1007/s10340-016-0774-3

    Article  Google Scholar 

  • Asplen MK, Anfora G, Biondi A et al (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494. https://doi.org/10.1007/s10340-015-0681-z

    Article  Google Scholar 

  • Boemare N (2002) Biology, taxonomy, and systematics of Photorhabdus and Xenorhabdus. In: Gaugler R (ed) Entomopathogenic nematology. CABI International, Wallingford, pp 35–56

    Chapter  Google Scholar 

  • Bruck DJ, Bolda M, Tanigoshi L et al (2011) Laboratory and field comparisons of insecticides to reduce infestation of Drosophila suzukii in berry crops. Pest Manag Sci 67:1375–1385. https://doi.org/10.1002/ps.2242

    Article  CAS  PubMed  Google Scholar 

  • Calabria G, Máca J, Bächli G et al (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147. https://doi.org/10.1111/j.1439-0418.2010.01583.x

    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 

  • Cuthbertson AGS, Audsley N (2016) Further screening of entomopathogenic fungi and nematodes as control agents for Drosophila suzukii. Insects 7:24. https://doi.org/10.3390/insects7020024

    Article  PubMed Central  Google Scholar 

  • Cuthbertson AGS, Collins DA, Blackburn LF, Audsley NA, Bell HA (2014) Preliminary screening of potential control products against Drosophila suzukii. Insects 5:488–498

    Article  Google Scholar 

  • Entling W, Anslinger S, Jarausch B, Michl G, Hoffmann C (2019) Berry skin resistance explains oviposition preferences of Drosophila suzukii at the level of grape cultivars and single berries. J Pest Sci 92:477–484. https://doi.org/10.1007/s10340-018-1040-7

    Article  Google Scholar 

  • Garcia-del-Pino F, Morton A (2001) Los nematodos entomopatógenos para el control biológico de la cucaracha alemana, Blattella germanica (Dictyoptera: Blattellidae). In: Proceedings of III Congreso Nacional de Entomología Aplicada Pamplona Spain 2001, p 122

  • Garcia-del-Pino F, Alabern X, Morton A (2013) Efficacy of soil treatments of entomopathogenic nematodes against the larvae, pupae and adults of Tuta absoluta and their interaction with the insecticides used against this insect. Biocontrol 58:723–731

    Article  CAS  Google Scholar 

  • Garriga A, Morton A, Garcia-del-Pino F (2018) Is Drosophila suzukii as susceptible to entomopathogenic nematodes as Drosophila melanogaster? J Pest Sci 91:789–798. https://doi.org/10.1007/s10340-017-0920-6

    Article  Google Scholar 

  • Geden CJ, Axtell RC, Brooks WM (1986) Susceptibility of the house fly, Musca domestica (Diptera: Muscidae), to the entomogenous nematodes Steinernema feltiae, S. glaseri (Steinernematidae), and Heterorhabditis heliothidis (Heterorhabditidae). J Med Entomol 23:326–332

    Article  CAS  Google Scholar 

  • Giorgini M, Wang XG, Wang Y et al (2019) Exploration for native parasitoids of Drosophila suzukii in China reveals a diversity of parasitoid species and narrow host range of the dominant parasitoid. J Pest Sci 92:509–522. https://doi.org/10.1007/s10340-018-01068-3

    Article  Google Scholar 

  • Goodhue RE, Bolda M, Farnsworth D et al (2011) Spotted wing drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Manag Sci 67:1396–1402. https://doi.org/10.1002/ps.2259

    Article  CAS  PubMed  Google Scholar 

  • Grewal PS, Ehlers R-U, Shapiro-Ilan DI (eds) (2005) Nematodes as biocontrol agents. CABI Publishing, Oxon, p 528

    Google Scholar 

  • Hamby KA, Bellamy DE, Chiu JC et al (2016) Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. J Pest Sci 89:605–619. https://doi.org/10.1007/s10340-016-0756-5

    Article  Google Scholar 

  • Heve WK, El-Borai FE, Carrillo D, Duncan LW (2017) Biological control potential of entomopathogenic nematodes for management of Caribbean fruit fly, Anastrepha suspensa Loew (Tephritidae). Pest Manag Sci 73(6):1220–1228. https://doi.org/10.1002/ps.4447

    Article  CAS  PubMed  Google Scholar 

  • Hübner A, Englert C, Herz A (2017) Effect of entomopathogenic nematodes on different developmental stages of Drosophila suzukii in and outside fruits. Biocontrol 62:669–680. https://doi.org/10.1007/s10526-017-9832-x

    Article  Google Scholar 

  • Ibouh K, Oreste M, Bubici G, Tarasco E, Rossi Stacconi MV, Ioriatti C, Verrastro V, Anfora G, Baser N (2019) Biological control of Drosophila suzukii: Efficacy of parasitoids, entomopathogenic fungi, nematodes and deterrents of oviposition in laboratory assays. Crop Prot. https://doi.org/10.1016/j.cropro.2019.104897

    Article  Google Scholar 

  • Kamali S, Karimi J, Hosseini M, Campos-Herrera R, Duncan LW (2013) Biocontrol potential of the entomopathogenic nematodes Heterorhabditis bacteriophora and Steinernema carpocapsae on cucurbit fly, Dacus ciliatus (Diptera: Tephritidae). Biocontrol Sci Technol 23(11):1307–1323

    Article  Google Scholar 

  • Kanzawa T (1939) Studies on Drosophila suzukii Mats. Yamanashi Agricultural Experimental Station, Kofu

    Google Scholar 

  • Kaya HK, Grieve BJ (1982) The nematode Neoaplectana carpocapsae and the beet armyworm Spodoptera exigua: infectivity of prepupae and pupae in soil and of adults during emergence from soil. J Invertebr Pathol 39:192–197

    Article  Google Scholar 

  • Kenis M, Tonina L, Eschen R et al (2016) Non-crop plants used as hosts by Drosophila suzukii in Europe. J Pest Sci 89:735–748. https://doi.org/10.1007/s10340-016-0755-6

    Article  Google Scholar 

  • Kim HH, Choo HY, Kaya HK, Lee DW, Lee SM, Jeon HY (2004) Steinernema carpocapsae (Rhabditida: Steinernematidae) as a biological control agent against the fungus Gnat Bradysia agrestis (Diptera: Sciaridae) in propagation houses. Biocontrol Sci Technol 14(2):171–183. https://doi.org/10.1080/09583150310001655693

    Article  Google Scholar 

  • Klein MG (1990) Efficacy against soil-inhabiting insects pest. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes biological control. CRC Press, Boca Raton, pp 195–214

    Google Scholar 

  • Leach H, Moses J, Hanson E, Fanning P, Isaacs R (2018) Rapid harvest schedules and fruit removal as non-chemical approaches for managing spotted wing Drosophila. J Pest Sci 91:219–226. https://doi.org/10.1007/s10340-017-0873-9

    Article  Google Scholar 

  • Lee JC, Bruck DJ, Dreves AJ et al (2011) In Focus: spotted wing drosophila, Drosophila suzukii, across perspectives. Pest Manag Sci 67:1349–1351. https://doi.org/10.1002/ps.2271

    Article  CAS  PubMed  Google Scholar 

  • Lee JC, Wang X, Daane KM, Hoelmer KA, Isaacs R, Sial AA, Walton VM (2019) Biological control of spotted-wing drosophila: current and pending tactics. J IPM 10(1):1–9. https://doi.org/10.1093/jipm/pmz012

    Article  Google Scholar 

  • Ma J, Chen S, Moens M et al (2013) Efficacy of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) against the chive gnat, Bradysia odoriphaga. J Pest Sci 86:551–561. https://doi.org/10.1007/s10340-013-0497-7

    Article  Google Scholar 

  • Mahmoud YA, Ebadah IA, Metwally HMS, Saleh ME (2016) Controlling of larvae, pupae and adults of the Peach fruit fly, Bactrocera zonata (Saund.) (Diptera: Tephritidae) with the entomopathogenic nematode. Steinernema feltiae. Egypt J Biol Pest Control 26(3):615–617

    Google Scholar 

  • Malan AP, Manrakhan A (2009) Susceptibility of Mediterranean fruit fly (Ceratitis capitata) and the Natal fruit fly (Ceratitis rosa) to entomopathogenic nematodes. J Invertebr Pathol 100:47–49. https://doi.org/10.1016/j.jip.2008.09.007

    Article  PubMed  Google Scholar 

  • Morton A, Garcia-del-Pino F (2007) Susceptibility of shore fly Scatella stagnalis to five entomopathogenic nematode strains in bioassays. Biocontrol 52:533–545. https://doi.org/10.1007/s10526-006-9047-z

    Article  Google Scholar 

  • Peabody NC, White BH (2013) Eclosion gates progression of the adult ecdysis sequence of Drosophila. J Exp Biol 216:4395–4402. https://doi.org/10.1242/jeb.091595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poinar GO Jr (1990) Biology and taxonomy of Steinernematidae and Heterorhabditidae. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, pp 23–62

    Google Scholar 

  • Poinar GO Jr, Hislop RG (1981) Mortality of Mediterranean fruit fly adults (Ceratitis capitata) from parasitic nematodes (Neoaplectana and Heterorhabditis spp.). IRCS Med Sci Biochem Dev Biol Med Microbiol Parasitol Infect Dis 9:641

    Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • Renkema JM, Cuthbertson AGS (2018) Impact of multiple natural enemies on immature Drosophila suzukii in strawberries and blueberries. Biocontrol 63:719–728. https://doi.org/10.1007/s10526-018-9874-8

    Article  Google Scholar 

  • San-Blas E, Gowen SR (2007) Facultative scavenging as a survival strategy of entomopathogenic nematodes. Int J Parasitol 38:85–91

    Article  Google Scholar 

  • Sánchez-Ramos I, Gómez-Casado E, Fernández CE, González-Núñez M (2019) Reproductive potential and population increase of Drosophila suzukii at constant temperaturas. Entomol Generalis 39(2):103–115. https://doi.org/10.1127/entomologia/2019/0794

    Article  Google Scholar 

  • Santoiemma G, Trivellato F, Caloi V, Mori N, Marini L (2019) Habitat preference of Drosophila suzukii across heterogeneous landscapes. J Pest Sci 92:485–494. https://doi.org/10.1007/s10340-018-1052-3

    Article  Google Scholar 

  • Tonina L, Mori N, Sancassani M et al (2018) Spillover of Drosophila suzukii between noncrop and crop areas: implications for pest management. Agric For Meteorol 20:575–581

    Google Scholar 

  • Walsh DB, Bolda MP, Goodhue RE et al (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:1–7. https://doi.org/10.1603/IPM10010

    Article  Google Scholar 

  • White GF (1927) A method for obtaining infective nematode larvae from cultures. Science 66:302–303

    Article  CAS  Google Scholar 

  • Woltz JM, Lee JC (2017) Pupation behavior and larval and pupal biocontrol of Drosophila suzukii in the field. Biol Control 110:62–69. https://doi.org/10.1016/j.biocontrol.2017.04.007

    Article  Google Scholar 

  • Wong JS, Cave AC, Lightle DM et al (2018) Drosophila suzukii flight performance reduced by starvation but not affected by humidity. J Pest Sci 91:1269–1278

    Article  Google Scholar 

  • Woodring JL, Kaya HK (1998) Steinernematid and heterorhabditid nematodes: a handbook of techniques. South Cooper Bull 331:1–30

    Google Scholar 

  • Yee LY, Lacey LA (2003) Stage-specific mortality of Rhagoletis indifferens (Diptera: Tephritidae) exposed to three species of Steinernema nematodes. Biol Control 27:349–356

    Article  Google Scholar 

  • Yousef M, Aranda-Valera E, Quesada-Moraga E (2018) Lure-and-infect and lure-and-kill devices based on Metarhizium brunneum for spotted wing Drosophila control. J Pest Sci 91:227–235. https://doi.org/10.1007/s10340-017-0874-8

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank to IRTA-Cabrils (Institut de Recerca i Tecnologia Agroalimentàries) for providing D. suzukii adults for culture.

Funding

This work was supported by FEDER/Ministerio de Ciencia, Innovación y Universidades—Agencia Estatal de Investigación/Project (AGL2017-86770-R).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fernando Garcia-del-Pino.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by A. Biondi.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garriga, A., Morton, A., Ribes, A. et al. Soil emergence of Drosophila suzukii adults: a susceptible period for entomopathogenic nematodes infection. J Pest Sci 93, 639–646 (2020). https://doi.org/10.1007/s10340-019-01182-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-019-01182-w

Keywords

Navigation