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First record of the invasive spotted wing Drosophila infesting berry crops in Africa

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Abstract

The spotted wing drosophila, Drosophila suzukii Matsumura (Diptera: Drosophilidae), is an invasive pest native to Asia that has recently invaded Europe and the Americas. This pest can seriously compromise fruit production in infested crops and has a remarkable ability to invade new areas with a diverse range of environments. We report for the first time D. suzukii infestations in African crops. We sampled 101 fields cultivated with soft-skinned fruits in two regions of northwestern Morocco. Morphological and molecular analyses confirmed the occurrence of D. suzukii in this area. In 2017 and 2018, approximately 15% of the surveyed farms growing small berries were infested by D. suzukii. A total of 61.11% of the surveyed raspberry fields were infested, followed by blueberries (22.22%), strawberries (11.11%) and mulberries (5.56%). Peak infestations were between March and June and in November and December. We carried out preliminary mass trapping in a raspberry tunnel, and of the two traps used, the red-colored trap baited with baker’s yeast and sugar was the most effective. The results are discussed in the light of the invasion potential for the African continent and integrated pest management (IPM) perspectives for soft fruit production in Morocco.

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References

  • 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

    Google Scholar 

  • Becher PG, Flick G, Rozpędowska E, Schmidt A, Hagman A et al (2012) Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development. Funct Ecol 26:822–828

    Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: Selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87(7):803–812

    CAS  PubMed  Google Scholar 

  • Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Annu Rev Entomol 63:239–258

    CAS  PubMed  Google Scholar 

  • Burrack HJ, Asplen M, Bahder L, Collins J, Drummond FA et al (2015) Multistate comparison of attractants for monitoring Drosophila suzukii (Diptera: Drosophilidae) in blueberries and caneberries. Environ Entomol 44:704–712

    PubMed  Google Scholar 

  • Calabria G, Maca J, Bachli G, Serra L, Pascual M (2010) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147

    Google Scholar 

  • Cloonan KR, Abraham J, Angeli S, Syed Z, Rodriguez-Saona C (2018) Advances in the chemical ecology of the spotted wing Drosophila (Drosophila suzukii) and its applications. J Chem Ecol 44:922–939

    CAS  PubMed  Google Scholar 

  • Delbac L, Rusch A, Thiéry D (2020) Temporal dynamics of Drosophila suzukii in vineyard landscapes. Entomologia Generalis

  • De la Vega GJ, Corley JC, Soliani C (2020) Genetic assessment of the invasion history of Drosophila suzukii in Argentina. J Pest Sci 93:63–75

    Google Scholar 

  • Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Ann Rev Entomol 52(1):81–106

    CAS  Google Scholar 

  • Dos Santos LA, Mendes MF, Krüger AP, Blauth ML, Gottschalk MS, Garcia FR (2017) Global potential distribution of Drosophila suzukii (Diptera, Drosophilidae). PLoS ONE 12(3):e0174318

    PubMed  PubMed Central  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

    Google Scholar 

  • Farnsworth D, Hamby K, Bolda M, Goodhue R, Williams J, Zalom F (2017) Economic analysis of revenue losses and control costs associated with the spotted wing drosophila, Drosophila suzukii (Matsumura), in the California raspberry industry. Pest Manag Sci 73:1083–1090

    CAS  PubMed  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 

  • Frewin AJ, Renkema J, Fraser H, Hallett RH (2017) Evaluation of attractants for monitoring Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 110:1156–1163

    PubMed  Google Scholar 

  • Garriga A, Morton A, Ribes A, Garcia-del-Pino F (2020) Soil emergence of Drosophila suzukii adults: a susceptible period for entomopathogenic nematodes infection. J Pest Sci 93:639–646

    Google Scholar 

  • Giorgini M, Wang XG, Wang Y, Chen FS, Hougardy E 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

    Google Scholar 

  • Goodhue RE, Bolda M, Farnsworth D, Williams JC, Zalom FG (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

    CAS  PubMed  Google Scholar 

  • Grumiaux C, Andersen MK, Colinet H, Overgaard J (2019) Fluctuating thermal regime preserves physiological homeostasis and reproductive capacity in Drosophila suzukii. J Insect Physiol 113:33–41

    CAS  PubMed  Google Scholar 

  • Guedes RNC, Cervantes FA, Backus EA, Walse SS (2019) Substrate-mediated feeding and egg-laying by spotted wing drosophila: waveform recognition and quantification via electropenetrography. J Pest Sci 92:495–507

    Google Scholar 

  • Gutierrez AP, Ponti L, Dalton DT (2016) Analysis of the invasiveness of spotted wing Drosophila (Drosophila suzukii) in North America, Europe, and the Mediterranean Basin. Biol Invasions 18:3647–3663

    Google Scholar 

  • Hamby KA, Becher PG (2016) Current knowledge of interactions between Drosophila suzukii and microbes, and their potential utility for pest management. J Pest Sci 89:621–630

    Google Scholar 

  • Hamby KA, Hernández A, Boundy-Mills K, Zaloma FG (2012) Associations of yeasts with spotted-wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in cherries and raspberries. Appl Environ Microbiol 78:4869–4873

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  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

    Google Scholar 

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

    Google Scholar 

  • Iglesias LE, Nyoike TW, Liburd OE (2014) Effect of trap design, bait type, and age on captures of Drosophila suzukii (Diptera: Drosophilidae) in berry crops. J Econ Entomol 107:1508–1518

    PubMed  Google Scholar 

  • Institute SAS (2008) SAS version 9.2. SAS Institute, Cary

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kirichenko N, Augustin S, Kenis M (2019) Invasive leafminers on woody plants: a global review of pathways, impact, and management. J Pest Sci 92(1):93–106

    Google Scholar 

  • Kirkpatrick DM, McGhee PS, Hermann SL, Gut LJ, Miller JR (2016) Alightment of spotted wing drosophila (Diptera: Drosophilidae) on odorless disks varying in color. Environ Entomol 45:185–191

    CAS  PubMed  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

    Google Scholar 

  • Lee JC, Bruck DJ, Curry H, Edwards DL, Haviland DR, Van Steenwyk R, Yorgey B (2011) The susceptibility of small fruits and cherries to the spotted wing drosophila, Drosophila suzukii. Pest Manag Sci 67:1358–1367

    CAS  PubMed  Google Scholar 

  • Lee JC, Shearer PW, Barrantes LD, Beers EH, Burrack HJ et al (2013) Trap designs for monitoring Drosophila suzukii (Diptera: Drosophilidae). Environ Entomol 42:1348–1355

    PubMed  Google Scholar 

  • Mansour R, Brévault T, Chailleux A, Cherif A, Grissa-Lebdi K et al (2018) Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomol Gen 38:83–112

    Google Scholar 

  • Markow TA, O’Grady PM (2008) Reproductive ecology of Drosophila. Funct Ecol 22:747–759

    Google Scholar 

  • Markow TA, O’Grady P (2006) Drosophila: a guide to species identification and use. Academic Press, Cambridge. ISBN: 0124730523, 9780124730526

  • 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

    PubMed Central  Google Scholar 

  • Medias24 (2019) https://www.medias24.com/la-production-nationale-de-fruits-rouges-en-forte-hausse-1147.html. Accessed 15 May 2020

  • Mendonca LDP, Oliveira EE, Andreazza F, Rezende SM, Faroni LRDA et al (2019) Host potential and adaptive responses of Drosophila suzukii (Diptera: Drosophilidae) to barbados cherries. J Econ Entomol 112:3002–3006

    PubMed  Google Scholar 

  • Miller ME, Marshall SA, Grimaldi DA (2017) A review of the species of Drosophila (Diptera: Drosophilidae) and genera of Drosophilidae of Northeastern North America. Can J Arthropod identif 31:1–282

    Google Scholar 

  • Mitsui H, Takahashi KH, Kimura MT (2006) Spatial distributions and clutch sizes of Drosophila species ovipositing on cherry fruits of different stages. Popul Ecol 48:233–237

    Google Scholar 

  • Navarro-Llopis V, Vacas S (2014) Mass trapping for fruit fly control. In: Shelly T, Epsky N, Jang EB, Reyes-Flores J, Vargas R (eds) Trapping and the detection, control, and regulation of tephritid fruit flies. Springer, Berlin, pp 513–555

    Google Scholar 

  • Nikolouli K, Sassù F, Mouton L, Stauffer C, Bourtzis K (2020) Combining sterile and incompatible insect techniques for the population suppression of Drosophila suzukii. J Pest Sci 93:647–661

    CAS  Google Scholar 

  • ONSSA (2018) Index phytosanitaire. http://eservice.onssa.gov.ma/IndPesticide.aspx. Accessed 15 May 2020

  • Paine MD (1996) Repeated measures designs. Environ Toxicol Chem Int J 15(9):1439–1441

    CAS  Google Scholar 

  • Philippe V, Neveen A, Marwa A, Ahmad Basel A-Y (forthcoming) Occurrence of pesticide residues in fruits and vegetables for the Eastern Mediterranean Region and potential impact on public health. Food Control 119:107457

  • Renkema JM, Buitenhuis R, Hallett RH (2014) Optimizing trap design and trapping protocols for Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 107:2107–2118

    PubMed  Google Scholar 

  • Rice K, Short B, Jones S, Leskey T (2016) Behavioral responses of Drosophila suzukii (Diptera: Drosophilidae) to visual stimuli under laboratory, semifield, and field conditions. Environ Entomol 45:1480–1488

    PubMed  Google Scholar 

  • Rossi-Stacconi MVR, Amiresmaeili N, Biondi A, Carli C et al (2018) Host location and dispersal ability of the cosmopolitan parasitoid Trichopria drosophilae released to control the invasive spotted wing Drosophila. Biol Control 117:188–196

    Google Scholar 

  • Rota-Stabelli O, Ometto L, Tait G, Ghirotto S, Kaur R et al (2020) Distinct genotypes and phenotypes in European and American strains of Drosophila suzukii: implications for biology and management of an invasive organism. J Pest Sci 93:77–89

    Google Scholar 

  • Saerens SMG, Delvaux FR, Verstrepen KJ, Thevelein JM (2010) Production and biological function of volatile esters in Saccharomyces cerevisiae. Microb Biotechnol 3:165–177

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sánchez-Ramos I, Fernández CE, González-Núñez M (2019a) Comparative analysis of thermal performance models describing the effect of temperature on the preimaginal development of Drosophila suzukii. J Pest Sci 92:523–541

    Google Scholar 

  • Sánchez-Ramos I, Gómez-Casado E, Fernández CE, González-Núñez M (2019b) Reproductive potential and population increase of Drosophila suzukii at constant temperatures. Entomol Gen 39:103–115

    Google Scholar 

  • Santana PA, Kumar L, Da Silva RS, Picanço MC (2019) Global geographic distribution of Tuta absoluta as affected by climate change. J Pest Sci 92(4):1373–1385

    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

    Google Scholar 

  • Santoiemma G, Tonina L, Marini L, Duso C, Mori N (2020) Integrated management of Drosophila suzukii in sweet cherry orchards. Entomol Gen. https://doi.org/10.1127/entomologia/2019/0947

    Article  Google Scholar 

  • Scheidler NH, Liu C, Hamby KA, Zalom FG, Syed Z (2015) Volatile codes: correlation of olfactory signals and reception in Drosophila-yeast chemical communication. Sci Rep 5:14059

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schetelig MF, Lee K-Z, Otto S, Talmann L, Stökl J, Degenkolb T, Vilcinskas A, Halitschke R (2018) Environmentally sustainable pest control options for Drosophila suzukii. J Appl Entomol 142:3–17

    Google Scholar 

  • Seebens H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE, Jeschke JM, Pagad S, Pyšek P, Winter M, Arianoutsou M, Bacher S, Blasius B, Brundu G, Capinha C, Celesti-Grapow L, Dawson W, Dullinger S, Fuentes N, Jäger H, Kartesz J, Kenis M, Kreft H, Kühn I, Lenzner B, Liebhold A, Mosena A, Moser D, Nishino M, Pearman D, Pergl J, Rabitsch W, Rojas-Sandoval J, Roques A, Rorke S, Rossinelli S, Roy HE, Scalera R, Schindler S, Štajerová K, Tokarska-Guzik B, van Kleunen M, Walker K, Weigelt P, Yamanaka T, Essl F (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8(1)

  • Spitaler U, Bianchi F, Eisenstecken D, Castellan I, Angeli S et al (2020) Yeast species affects feeding and fitness of Drosophila suzukii adults. J Pest Sci 93:1295–1309

    Google Scholar 

  • Sylla S, Brévault T, Monticelli LS, Diarra K, Desneux N (2019) Geographic variation of host preference by the invasive tomato leaf miner Tuta absoluta: implications for host range expansion. J Pest Sci 92:1387–1396

    Google Scholar 

  • Tait G, Cabianca A, Grassi A, Pfab F, Oppedisano T, Puppato S, Mazzoni V, Anfora G, Walton V (2020) Drosophila suzukii daily dispersal between distinctly different habitats. Entomol Gen 40:25–47

    Google Scholar 

  • Tochen S, Dalton DT, Wiman NG, Hamm C, Shearer PW, Walton VM (2014) Temperature related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environ Entomol 43:501–510

    PubMed  Google Scholar 

  • Tonina L, Grassi A, Caruso S, Mori N, Gottardello A, Anfora G, Giomi F, Vaccari G, Ioriatti C (2018) Comparison of attractants for monitoring Drosophila suzukii in sweet cherry orchards in Italy. J Appl Entomol 142:1–8

    Google Scholar 

  • Vlach J (2013) Identifying Drosophila suzukii version from October 7, 2013. Oregon Department of Agriculture, Salem

    Google Scholar 

  • von Ende CN (1993) Repeated-measures analysis: growth and other time-dependent measures. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New York, pp 113–137

    Google Scholar 

  • Wang XG, Kaçar G, Biondi A, Daane KM (2016) Foraging efficiency and outcomes of interactions of two pupal parasitoids attacking the invasive spotted wing drosophila. Biol Control 96:64–71

    Google Scholar 

  • Weber DC, Ferro DN (1991) Non target noctuids complicate integrated pest management monitoring of sweet corn with pheromone traps in Massachusetts. J Econ Entomol 84:1364–1369

    Google Scholar 

  • Wiman NG, Dalton DT, Anfora G, Biondi A, Chiu JC et al (2016) Drosophila suzukii population response to environment and management strategies. J Pest Sci 89:653–665

    Google Scholar 

  • Wolf S, Boycheva-Woltering S, Romeis J, Collatz J (2020) Trichopria drosophilae parasitizes Drosophila suzukii in seven common non-crop fruits. J Pest Sci 93:627–638

    Google Scholar 

  • Zeng J, Liu Y, Zhang H, Liu J, Jiang Y, Wyckhuys KAG, Wu K (2020) Global warming modifies long-distance migration of an agricultural insect pest. J Pest Sci 93(2):569–581

    Google Scholar 

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Acknowledgements

The survey was carried out by the means of the National School of Agriculture of Meknes (ENA). Mass trapping has been kindly funded by ELITE HARVEST.

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Boughdad, A., Haddi, K., El Bouazzati, A. et al. First record of the invasive spotted wing Drosophila infesting berry crops in Africa. J Pest Sci 94, 261–271 (2021). https://doi.org/10.1007/s10340-020-01280-0

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