Biology:Drosophila suzukii

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Short description: Species of fly

Drosophila suzukii
DrosophilasuzukiiphotoMcEvey.jpg
Male and female
Scientific classification edit
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Diptera
Family: Drosophilidae
Genus: Drosophila
Subgenus: Sophophora
Species group: melanogaster
Species subgroup: suzukii
Species:
D. suzukii
Binomial name
Drosophila suzukii
(Matsumura, 1931)[1]

Drosophila suzukii, commonly called the spotted wing drosophila or SWD, is a fruit fly. D. suzukii, originally from southeast Asia, is becoming a major pest species in America and Europe, because it infests fruit early during the ripening stage, in contrast with other Drosophila species that infest only rotting fruit.[2]

Native to east Asia, D. suzukii was first described in 1931 by Shōnen Matsumura, it was observed in Japan as early as 1916 by T. Kanzawa.[3]

D. suzukii is a fruit crop pest and is a serious economic threat to soft summer fruit; i.e., cherries, blueberries, raspberries, blackberries, peaches, nectarines, apricots, grapes, and others.[4] Research investigating the specific threat D. suzukii poses to these fruit is ongoing.[5]

Description

Like other members of the Drosophilidae, D. suzukii is small, approximately 2 to 3.5 millimetres (5⁄64 to 9⁄64 in) in length and 5 to 6.5 millimetres (13⁄64 to 1⁄4 in) in wingspan [3] and looks like its fruit and vinegar fly relatives. Its body is yellow to brown with darker bands on the abdomen and it has red eyes. The male has a distinct dark spot near the tip of each wing; females do not have the spotted wing. The foreleg of the male sports dark bands on the first and second tarsi. The female has a long, sharp, serrated ovipositor.[6] The larvae are small, white, and cylindrical reaching 3.5 millimetres (9⁄64 in) in length.[4]

When first observed in a new region, D. suzukii has often been confused with the western cherry fruit fly (Rhagoletis indifferens) and was given the short-lasting name cherry vinegar fly.[7] The cherry fruit fly is significantly larger than D. suzukii (up to 5 millimetres (13⁄64 in)) and has a pattern of dark bands on its wings instead of the telltale spot of D. suzukii. The telltale spots on the wings of male D. suzukii have earned it the common name "spotted wing drosophila" (SWD).

Unlike its vinegar fly relatives which are primarily attracted to rotting or fermented fruit, female D. suzukii attack fresh, ripe fruit by using their saw-like ovipositor to lay eggs under the fruit's soft skin. The larvae hatch and grow in the fruit, destroying the fruit's commercial value. Economic impacts are significant; losses from large scale infestation (20% loss) across the US alone could equate to farm gate impacts > $500M.[8][9]

D. suzukii has a slow rate of evolution due to its lower number of generations per year, because it enters winter diapause.[10]

Distribution

Native to southeast Asia, D. suzukii was first described in 1931 by Matsumura. Observed in Japan as early as 1916 by T. Kanzawa,[3] it was widely observed throughout parts of Japan , Korea, and China by the early 1930s.[3] By the 1980s, the "fruit fly" with the spotted wings was seen in Hawaii. It first appeared in North America in central California in August 2008,[4] then was found in Oregon and Washington (state) by Lee et al., 2011[11](p369) in the Pacific Northwest in 2009,[12] and is now widespread throughout California's coastal counties,[9] western Oregon, western Washington,[4] and parts of British Columbia[13] and Florida.[14] During the summer of 2010 the fly was discovered for the first time in South Carolina, North Carolina,[15] Louisiana,[16] and Utah.[17] In Fall 2010 the fly was also discovered in Michigan[18] and Wisconsin.[19] The fly was first discovered in the northeastern states in 2011[20] and in Minnesota[21] and Idaho[11](p369) in 2012. As D. suzukii continues to spread, most of the states will most likely observe it. The pest has also been found in Europe, including the countries of Belgium, Italy, France , and Spain .[22][23]

Lifecycle

The lifespan of D. suzukii varies greatly between generations; from a few weeks to ten months.[3] Generations hatched early in the year have shorter lifespans than generations hatched after September.[3] Research shows that many of the males and most of the females of the late-hatching generations overwinter in captivity—some living as long as 300 days. Only adults overwinter successfully in the research conducted thus far. In Washington state, D. suzukii has been observed in association with two exotic and well-established species of blackberry, Rubus armeniacus (= Rubus discolor) and Rubus laciniatus (the Himalayan and Evergreen Blackberries, respectively.).[4] The fly has been observed reproducing on many other species of soft-skinned wild fruit, however, research is still ongoing to determine the quality of individual species as reproductive hosts.

Adults emerge from overwintering when temperatures reach approximately 10 °C (50 °F) (and 268 degree days).[4] The fertilized female searches for ripe fruit, lands on the fruit, inserts its serrated ovipositor to pierce the skin and deposits a clutch of 1 to 3 eggs per insertion. Females will oviposit on many fruits and in regions of scarce fruit, many females will oviposit on the same fruit. In captivity in Japan, research shows up to 13 generations of D. suzukii may hatch per season. A female may lay as many as 300 eggs during its lifespan. With as many as 13 generations per season, and the ability for the female to lay up to 300 eggs each, the potential population size of D. suzukii is huge. It is also important to note that males of D. suzukii become sterile at 30 °C (86 °F) and population size may be limited in regions that reach that temperature.

The larvae grow inside the fruit. The oviposition site is visible in many fruit by a small pore scar in the skin of the fruit often called a "sting". After 1 or 2 days, the area around the "sting" softens and depresses creating an increasingly visible blemish.[4] The depressions may also exude fluid which may attract infection by secondary bacterial and fungal pathogens.[9] Larvae may leave the fruit, or remain inside it, to pupate.

Economic impact

The economic impact of D. suzukii on fruit crops is negative and significantly affects a wide variety of summer fruit in the United States including cherries,[9][11](p369) blueberries,[9][11](p369) grapes,[9] nectarines,[9] pears,[9] plums,[9] pluots,[9] peaches,[9] raspberries,[11](p369) and strawberries,[9] and blackberries.[11](p369) Damage was first noticed in North America in the western states of California, Oregon, and Washington in 2008; yield loss estimates from that year vary widely, with negligible loss in some areas to 80% loss in others depending on location and crop.[9] The $500 million actual loss due to pest damage in 2008—the first year D. suzukii was observed in California—is an indication of the potential damage the pest can cause upon introduction to a new location. Economic losses have now been reported across North America and in Europe as the fly has spread to new areas. In 2015 it is estimated that national economic loss for producers in the United States was $700 million.[24] Future losses may decrease as growers learn how to better control the pest, or may keep increasing as the fly continues to spread.

Agricultural management

Red plastic cup used as a homemade trap for monitoring

Due to the impact of D. suzukii on soft fruits, farmers have started to monitor and control it. There are different types of traps, both commercial and home-made, that are effective in monitoring it. Traps that use apple cider vinegar with a bait made of whole wheat dough have been successful for farmers for both capture and monitoring.[25] Farmers are advised to place these traps in a shaded area as soon as the first fruit is set and to not remove them until the end of harvest. The traps should be checked once a week and farmers should look for the spot on the wing of the males to determine if D. suzukii is present.[26]

In areas where D. suzukii has already been established or where its activity has been monitored, there are different ways to control it. One way to manage D. suzukii is to remove the infested fruit and place it in a plastic bag in the garbage. This method is effective from removing D. suzukii from gardens and small areas but is difficult for farmers with larger operations to do this. Farmers can also harvest their soft fruit early which reduces the exposure of fruit to D. suzukii and the likelihood of damage.[27]

Farmers have the option of both conventional and organic sprays[28] to control D. suzukii. Timing of the sprays is important to effectively controlling it. Since D. suzukii is more active in the morning and evening those are the best times to control it.[29] Sprays should be in place prior to egg laying and the coverage needs to be thorough because adults often hide in dense portion of the canopy. Depending on the variety of soft fruit and laws in different states and countries, there are many types of organic and conventional sprays that are effective. Different laws and pre-harvest date intervals need to be kept in mind when choosing a type of spray. Most types of sprays need to be applied each week, at a minimum. To prevent resistance to certain sprays, farmers must rotate among different insecticides.[30]

Parasitoids

Genetic engineering

There is ongoing research into population control methods using gene editing. Since 2017, biotechnology startup Agragene has been developing an approach that uses CRISPR on fly embryos to knock out two genes—one that sterilizes male flies, the other which prevents the females from hatching. Once hatched, the male flies would be released to mate with wild females, who would then lay sterile eggs. The company estimates releasing four to five sterile males to every one wild male per generation would be necessary to control a population. Because of the species' short lifespan, multiple weekly releases per season could be required for an effective deterrent. In May 2023, USDA and company researchers began greenhouse testing of the technique with the aim of deploying field tests in 2024.[39][40]

Researchers at North Carolina State University have been developing a technique that also uses CRISPR to modify a gene essential to female sexual development that renders them unable to lay eggs. The male flies, however, remain fertile and pass the mutated gene to future generations when they mate with unmodified females. This has the potential benefit of not requiring multiple releases like the Agragene method does. The researchers estimate that a release of one modified fly to every four wild flies would control populations within 10 generations, or about 20 weeks.[39][41][42]

Predators

Earwigs,[43] damsel bugs,[43] spiders,[43] ants,[43] and Orius ("minute pirate bugs")[43] especially O. insidiosus.[43][44] Likely also ground beetles (Carabidae),[43] crickets,[43] green lacewings' larvae,[43] rove beetles (Staphylinidae) especially Dalotia coriaria,[43] birds,[43][45] and mammals.[43][45]

Microbiome

Drosophila suzukii, like all insects, is host to a variety of microorganisms. The intestinal bacterial communities of adult and larval D. suzukii collected in its invasive range (USA), were found to be simple and mostly dominated by Tatumella spp. (Enterobacteriaceae).[46] This fly is also infected with a variety of viruses in the wild. Whilst sharing some natural viruses with its close relative D. melanogaster, D. suzukii also harbours a number of unique viruses specific to it alone.[47] Yeasts also form an important part of the Drosophila microbiome, with a mutualistic relationships to yeast being described in other Drosophila species.[48][49][50] The yeast species found to be most frequently associated with D. suzukii were Hanseniaspora uvarum, Metschnikowia pulcherrima, Pichia terricola, and P. kluyveri.[51] Although certain fungal pathogens have been shown to experimentally infect D. suzukii,[52][53][54] the wild fungal infections of D. suzukii remain to be explored comprehensively.

Gallery

  • Male, note the dark spots near his wing tips

  • Female, her wings are without spots

  • Male

  • Electron microscope image of the ovipositor of a female

  • Cherry with oviposition scars

  • Larva under compound microscope

References

  1. ↑ Matsumura, S. (1931) (in ja). 6000 illustrated insects of Japan-Empire. Tokyo, Japan: Toko Shoin. pp. 1689 [367]. http://dl.ndl.go.jp/info:ndljp/pid/1145547. 
  2. ↑ Walsh, Douglas B.; Bolda, Mark P.; Goodhue, Rachael E.; Dreves, Amy J.; Lee, Jana; Bruck, Denny J.; Walton, Vaughn M.; O'Neal, Sally D. et al. (2011). "Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential". Journal of Integrated Pest Management 2 (1): G1–G7. doi:10.1603/IPM10010. 
  3. ↑ 3.0 3.1 3.2 3.3 3.4 3.5 Kanzawa, T. 1939 Report. Translated from Japanese by Shinji Kawaii
  4. ↑ 4.0 4.1 4.2 4.3 4.4 4.5 4.6 Walsh, D. Press Release, Washington State University. 2009
  5. ↑ Herring, P. Grant funds help regional effort to combat spotted wing drosophila. 29 April 2010. http://extension.oregonstate.edu/news/story.php?S_No=729&storyType=news.
  6. ↑ McEvey, Shane (13 February 2017). High resolution diagnostic images of Drosophila suzukii (Diptera: Drosophilidae). Figshare. doi:10.6084/m9.figshare.4644793.v1. 
  7. ↑ Spotted Wing Drosophila, Drosophila suzukii: A New Pest in California. UC IPM Online, 10 Apr 2010. http://www.ipm.ucdavis.edu/EXOTIC/drosophila.html
  8. ↑ Fountain, Michelle T.; Badiee, Amir; Hemer, Sebastian; Delgado, Alvaro; Mangan, Michael; Dowding, Colin; Davis, Frederick; Pearson, Simon (2020). "The use of light spectrum blocking films to reduce populations of Drosophila suzukii Matsumura in fruit crops". Scientific Reports 10 (1): 15358. doi:10.1038/s41598-020-72074-8. PMID 32958797. Bibcode: 2020NatSR..1015358F. 
  9. ↑ 9.00 9.01 9.02 9.03 9.04 9.05 9.06 9.07 9.08 9.09 9.10 9.11 9.12 Bolda, Mark P.; Goodhue, Rachael E.; Zalom, Frank G. (January–February 2010). "Spotted Wing Drosophila: Potential Economic Impact of Newly Established Pest". Agricultural and Resource Economics Update (ARE Update) (Giannini Foundation of Agricultural Economics, University of California) 13 (3): 5–8. http://giannini.ucop.edu/filer/file/1453327753/16824/. 
  10. ↑ Ometto, Lino; Cestaro, Alessandro; Ramasamy, Sukanya; Grassi, Alberto; Revadi, Santosh; Siozios, Stefanos; Moretto, Marco; Fontana, Paolo et al. (2013-03-15). "Linking Genomics and Ecology to Investigate the Complex Evolution of an Invasive Drosophila Pest". Genome Biology and Evolution (Oxford University Press (OUP)) 5 (4): 745–757. doi:10.1093/gbe/evt034. ISSN 1759-6653. PMID 23501831. 
  11. ↑ 11.0 11.1 11.2 11.3 11.4 11.5 Poland, Therese M., ed (2021). Invasive Species in Forests and Rangelands of the United States. Cham, Switzerland: Springer International Publishing. pp. xlii + 455 + ill., 20 b/w + 67 col. ISBN 978-3-030-45366-4.  ISBN 978-3-030-45369-5 ISBN 978-3-030-45367-1
  12. ↑ "Stop The Invasion - Spotted Wing Drosophila". 2017. http://invasivespecies.wa.gov/wp-content/uploads/2019/07/SpottedWingDrosophila-FactSheet.pdf. ""They’re known to have been in the Pacific Northwest since 2009."" 
  13. ↑ Spotted Wing Drosophila (Fruit Fly) Pest Alert. British Columbia Ministry of Agriculture and Lands. December 2009. http://www.agf.gov.bc.ca/cropprot/swd.htm
  14. ↑ Steck, G, Dixon, W, Dean, D. Pest Alert, Spotted Wing Drosophila, a fruit pest new to North America. 2009
  15. ↑ Spotted Wing Drosophila. NC Small Fruit, Specialty Crop, and Tobacco IPM. 2010. http://ncsmallfruitsipm.blogspot.com/p/spotted-wing-drosophila.html
  16. ↑ "Spotted Wing Drosophila". Louisiana Department of Agriculture and Forestry. August 2010. http://www.ldaf.state.la.us/portal/Portals/0/AES/Horticulture/Quarantine_programs/Spotted%20Wing%20Drosophila%20Profile.pdf. 
  17. ↑ Davis, R., Alston, D., Vorel, C. Spotted Wing Drosophila September 2010. http://extension.usu.edu/files/publications/publication/ENT-140-10.pdf
  18. ↑ "Early detection program finds a new invasive pest of fruit in Michigan". 29 Oct 2010. http://www.ipmnews.msu.edu/fruit/Fruit/tabid/123/articleType/ArticleView/articleId/3202/Early-detection-program-finds-a-new-invasive-pest-of-fruit-in-Michigan.aspx. 
  19. ↑ Hamilton, K. Wisconsin Pest Bulletin. 19 November 2010
  20. ↑ "Spotted Wing Drosophila IPM Working Group" (in en-US). 2012-11-13. http://www.northeastipm.org/working-groups/spotted-wing-drosophila/. 
  21. ↑ "Spotted Wing Drosophila | Minnesota Department of Agriculture". https://www.mda.state.mn.us/plants-insects/spotted-wing-drosophila. 
  22. ↑ Belgian Journal of Zoology - Drosophila suzukii (Diptera: Drosophilidae): A pest species new to Belgium. - Link
  23. ↑ Drosophila suzukii (Diptera: Drosophilidae): Spotted wing drosophila. European and Mediterranean Plant Protection Organization. January 2010. http://www.eppo.org/QUARANTINE/Alert_List/insects/drosophila_suzukii.htm
  24. ↑ "USDA Awards $6.7 Million To Stifle Spotted Wing Drosophila" (in en-US). 2015-10-20. https://www.growingproduce.com/fruits/berries/usda-awards-6-7-million-to-stifle-spotted-wing-drosophila/. 
  25. ↑ "Monitoring | Cornell Fruit Resources". http://fruit.cornell.edu/spottedwing/monitoring/. 
  26. ↑ "Spotted wing drosophila in home gardens" (in en). https://extension.umn.edu/yard-and-garden-insects/spotted-wing-drosophila. 
  27. ↑ "Spotted Wing Drosophila Management Guidelines--UC IPM". http://ipm.ucanr.edu/PMG/PESTNOTES/pn74158.html. 
  28. ↑ Dam, Doriane; Molitor, Daniel; Beyer, Marco (2019). "Natural compounds for controlling Drosophila suzukii" (in en). Agronomy for Sustainable Development 39 (6). doi:10.1007/s13593-019-0593-z. 
  29. ↑ "New guide to organic management of spotted wing Drosophila released" (in en). 19 June 2018. https://www.canr.msu.edu/news/new-guide-to-organic-management-of-spotted-wing-drosophila-released. 
  30. ↑ "Spotted Wing Drosophila Management | Entomology". https://entomology.ca.uky.edu/ef230. 
  31. ↑ "SWD-killing wasps to make their debut". 23 November 2020. http://www.goodfruit.com/swd-killing-wasps-to-make-their-debut/. 
  32. ↑ 32.00 32.01 32.02 32.03 32.04 32.05 32.06 32.07 32.08 32.09 32.10 32.11 Daane, Kent M.; Wang, Xin-Geng; Biondi, Antonio; Miller, Betsey; Miller, Jeffrey C.; Riedl, Helmut; Shearer, Peter W.; Guerrieri, Emilio et al. (2016-02-10). "First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents". Journal of Pest Science (Springer Science and Business Media LLC) 89 (3): 823–835. doi:10.1007/s10340-016-0740-0. ISSN 1612-4758. 
  33. ↑ 33.00 33.01 33.02 33.03 33.04 33.05 33.06 33.07 33.08 33.09 33.10 33.11 33.12 Giorgini, Massimo; Wang, Xin-Geng; Wang, Yan; Chen, Fu-Shou; Hougardy, Evelyne; Zhang, Hong-Mei; Chen, Zong-Qi; Chen, Hong-Yin et al. (2018-12-12). "Exploration for native parasitoids of Drosophila suzukii in China reveals a diversity of parasitoid species and narrow host range of the dominant parasitoid". Journal of Pest Science (Springer Science and Business Media LLC) 92 (2): 509–522. doi:10.1007/s10340-018-01068-3. ISSN 1612-4758. 
  34. ↑ 34.0 34.1 Girod, Pierre; Borowiec, Nicolas; Buffington, Matthew; Chen, Guohua; Fang, Yuan; Kimura, Masahito T.; Peris-Felipo, Francisco Javier; Ris, Nicolas et al. (2018-08-07). "The parasitoid complex of D. suzukii and other fruit feeding Drosophila species in Asia". Scientific Reports (Springer Science and Business Media LLC) 8 (1): 11839. doi:10.1038/s41598-018-29555-8. ISSN 2045-2322. PMID 30087364. Bibcode: 2018NatSR...811839G. 
  35. ↑ Nomano, Fumiaki Y.; Kasuya, Nazuki; Matsuura, Akira; Suwito, Awit; Mitsui, Hideyuki; Buffington, Matthew L.; Kimura, Masahito T. (2017-05-03). "Genetic differentiation of Ganaspis brasiliensis (Hymenoptera: Figitidae) from East and Southeast Asia". Applied Entomology and Zoology (Springer Science and Business Media LLC) 52 (3): 429–437. doi:10.1007/s13355-017-0493-0. ISSN 0003-6862. Bibcode: 2017AppEZ..52..429N. 
  36. ↑ 36.0 36.1 36.2 "ASIAN GIANT HORNET STAKEHOLDER UPDATE #17 – DECEMBER 9, 2020". http://cms.agr.wa.gov/WSDAKentico/Documents/PP/PestProgram/AGHStakeholderUpdate17.pdf. ""the traps also captured the first United States specimens of parasitoid wasps that prey on SWD. The parasitoid larvae will live off SWD and eventually kill it. Without these traps this parasitoid wasp might have gone unnoticed. This information may help the development of biological control programs to potentially help manage SWD."" 
  37. ↑ 37.0 37.1 37.2 "Murder Hornet traps yield bonus". 2020-12-16. http://kgmi.com/news/007700-murder-hornet-traps-yield-bonus/. 
  38. ↑ 38.0 38.1 38.2 "Catching hope: Possible ally in fight against harmful fruit fly discovered in Asian giant hornet trap". 14 December 2020. http://wastatedeptag.blogspot.com/2020/12/wasp.html. 
  39. ↑ 39.0 39.1 Mullin, Emily (June 29, 2023). "Scientists Are Gene-Editing Flies to Fight Crop Damage" (in en-US). Wired. ISSN 1059-1028. https://www.wired.com/story/gene-editing-flies-to-fight-crop-damage/. Retrieved June 29, 2023. 
  40. ↑ Rubbelke, Nathan (March 9, 2023). "Agtech startup Agragene relocates from San Diego to St. Louis, bringing with it thousands of fruit flies". https://www.bizjournals.com/stlouis/inno/stories/profiles/2023/03/09/agragene-st-louis-relocation-pest-control.html. 
  41. ↑ Walling, Melina (June 14, 2023). "To fight berry-busting fruit flies, researchers focus on sterilizing the bugs" (in en). https://apnews.com/article/fruit-flies-research-gene-drive-agriculture-b44315bfb21b7ce62c0e815797f60177. 
  42. ↑ Yadav, Amarish K.; Butler, Cole; Yamamoto, Akihiko; Patil, Anandrao A.; Lloyd, Alun L.; Scott, Maxwell J. (2023-06-20). "CRISPR/Cas9-based split homing gene drive targeting doublesex for population suppression of the global fruit pest Drosophila suzukii" (in en). Proceedings of the National Academy of Sciences 120 (25): e2301525120. doi:10.1073/pnas.2301525120. ISSN 0027-8424. PMID 37307469. Bibcode: 2023PNAS..12001525Y. 
  43. ↑ 43.00 43.01 43.02 43.03 43.04 43.05 43.06 43.07 43.08 43.09 43.10 43.11 Lee, Jana C; Wang, Xingeng; Daane, Kent M; Hoelmer, Kim A; Isaacs, Rufus; Sial, Ashfaq A; Walton, Vaughn M (2019-01-01). "Biological Control of Spotted-Wing Drosophila (Diptera: Drosophilidae)—Current and Pending Tactics". Journal of Integrated Pest Management (Oxford University Press (OUP)) 10 (1): 13. doi:10.1093/jipm/pmz012. ISSN 2155-7470. 
  44. ↑ Renkema, Justin M.; Cuthbertson, Andrew G. S. (2018-03-03). "Impact of multiple natural enemies on immature Drosophila suzukii in strawberries and blueberries". BioControl (Springer Science and Business Media LLC) 63 (5): 719–728. doi:10.1007/s10526-018-9874-8. ISSN 1386-6141. Bibcode: 2018BioCo..63..719R. 
  45. ↑ 45.0 45.1 Ballman, Elissa S; Collins, Judith A; Drummond, Francis A (2017-09-27). "Pupation Behavior and Predation on Drosophila suzukii (Diptera: Drosophilidae) Pupae in Maine Wild Blueberry Fields". Journal of Economic Entomology (Oxford University Press (OUP)) 110 (6): 2308–2317. doi:10.1093/jee/tox233. ISSN 0022-0493. PMID 29029219. 
  46. ↑ Chandler, James Angus; James, Pamela M.; Jospin, Guillaume; Lang, Jenna M. (2014-07-22). "The bacterial communities of Drosophila suzukii collected from undamaged cherries". PeerJ 2: e474. doi:10.7717/peerj.474. ISSN 2167-8359. PMID 25101226. 
  47. ↑ Medd, Nathan C; Fellous, Simon; Waldron, Fergal M; Xuéreb, Anne; Nakai, Madoka; Cross, Jerry V; Obbard, Darren J (2018-01-01). "The virome of Drosophila suzukii, an invasive pest of soft fruit". Virus Evolution 4 (1): vey009. doi:10.1093/ve/vey009. PMID 29644097. 
  48. ↑ Anagnostou, Christiana; Dorsch, Monika; Rohlfs, Marko (2010-07-01). "Influence of dietary yeasts on Drosophila melanogaster life-history traits". Entomologia Experimentalis et Applicata 136 (1): 1–11. doi:10.1111/j.1570-7458.2010.00997.x. ISSN 1570-7458. Bibcode: 2010EEApp.136....1A. 
  49. ↑ Starmer, William T. (1981-01-01). "A comparison of Drosophila habitats according to the physiological attributes of the associated yeast communities". Evolution 35 (1): 38–52. doi:10.1111/j.1558-5646.1981.tb04856.x. ISSN 1558-5646. PMID 28563455. 
  50. ↑ Simmons, Fred H; Bradley, Timothy J (1997). "An analysis of resource allocation in response to dietary yeast in Drosophila melanogaster". Journal of Insect Physiology 43 (8): 779–788. doi:10.1016/s0022-1910(97)00037-1. PMID 12770456. 
  51. ↑ Hamby, Kelly A.; Hernández, Alejandro; Boundy-Mills, Kyria; Zalom, Frank G. (2012-07-15). "Associations of Yeasts with Spotted-Wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in Cherries and Raspberries". Applied and Environmental Microbiology 78 (14): 4869–4873. doi:10.1128/aem.00841-12. ISSN 0099-2240. PMID 22582060. Bibcode: 2012ApEnM..78.4869H. 
  52. ↑ Woltz, J. M.; Donahue, K. M.; Bruck, D. J.; Lee, J. C. (2015-12-01). "Efficacy of commercially available predators, nematodes and fungal entomopathogens for augmentative control of Drosophila suzukii". Journal of Applied Entomology 139 (10): 759–770. doi:10.1111/jen.12200. ISSN 1439-0418. 
  53. ↑ Cuthbertson, Andrew G. S.; Collins, Debbie A.; Blackburn, Lisa F.; Audsley, Neil; Bell, Howard A. (2014-06-20). "Preliminary Screening of Potential Control Products against Drosophila suzukii". Insects 5 (2): 488–498. doi:10.3390/insects5020488. PMID 26462696. 
  54. ↑ Becher, Paul G.; Jensen, Rasmus E.; Natsopoulou, Myrsini E.; Verschut, Vasiliki; Licht, Henrik H. De Fine (2018-03-01). "Infection of Drosophila suzukii with the obligate insect-pathogenic fungus Entomophthora muscae". Journal of Pest Science 91 (2): 781–787. doi:10.1007/s10340-017-0915-3. ISSN 1612-4758. PMID 29568251. 

External links

Further reading

Wikidata ☰ Q1336450 entry



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