Drosophila suzukii

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Drosophila suzukii
DrosophilasuzukiiphotoMcEvey.jpg
Male and female
Scientific classification OOjs UI icon edit-ltr.svg
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]

Contents

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] : 369  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] : 369  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] : 369  blueberries, [9] [11] : 369  grapes, [9] nectarines, [9] pears, [9] plums, [9] pluots, [9] peaches, [9] raspberries, [11] : 369  and strawberries, [9] and blackberries. [11] : 369  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 Spotted Wing Drosophila Trap.jpg
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.

Related Research Articles

<i>Drosophila</i> Genus of flies

Drosophila is a genus of flies, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or pomace flies, vinegar flies, or wine flies, a reference to the characteristic of many species to linger around overripe or rotting fruit. They should not be confused with the Tephritidae, a related family, which are also called fruit flies ; tephritids feed primarily on unripe or ripe fruit, with many species being regarded as destructive agricultural pests, especially the Mediterranean fruit fly.

<span class="mw-page-title-main">Fly</span> Order of insects

Flies are insects of the order Diptera, the name being derived from the Greek δι- di- "two", and πτερόν pteron "wing". Insects of this order use only a single pair of wings to fly, the hindwings having evolved into advanced mechanosensory organs known as halteres, which act as high-speed sensors of rotational movement and allow dipterans to perform advanced aerobatics. Diptera is a large order containing an estimated 1,000,000 species including horse-flies, crane flies, hoverflies, mosquitoes and others, although only about 125,000 species have been described.

<i>Drosophila melanogaster</i> Species of fruit fly

Drosophila melanogaster is a species of fly in the family Drosophilidae. The species is often referred to as the fruit fly or lesser fruit fly, or less commonly the "vinegar fly", "pomace fly", or "banana fly". Starting with Charles W. Woodworth's 1901 proposal of the use of this species as a model organism, D. melanogaster continues to be widely used for biological research in genetics, physiology, microbial pathogenesis, and life history evolution. As of 2017, six Nobel Prizes have been awarded to drosophilists for their work using the insect.

<span class="mw-page-title-main">Drosophilidae</span> Family of flies

The Drosophilidae are a diverse, cosmopolitan family of flies, which includes species called fruit flies, although they are more accurately referred to as vinegar or pomace flies. Another distantly related family of flies, Tephritidae, are true fruit flies because they are frugivorous, and include apple maggot flies and many pests. The best known species of the Drosophilidae is Drosophila melanogaster, within the genus Drosophila, also called the "fruit fly." Drosophila melanogaster is used extensively for studies concerning genetics, development, physiology, ecology and behaviour. Many fundamental biological mechanisms were discovered first in D. melanogaster. The fruit fly is mostly composed of post-mitotic cells, has a very short lifespan, and shows gradual aging. As in other species, temperature influences the life history of the animal. Several genes have been identified that can be manipulated to extend the lifespan of these insects. Additionally, Drosophila subobscura, also within the genus Drosophila, has been reputed as a model organism for evolutionary-biological studies, along with D. sechellia for the evolution of host specialization on the toxic noni fruit and Scaptomyza flava for the evolution of herbivory and specialist on toxic mustard leaves.

<span class="mw-page-title-main">Tephritidae</span> Family of fruit flies

The Tephritidae are one of two fly families referred to as fruit flies, the other family being the Drosophilidae. The family Tephritidae does not include the biological model organisms of the genus Drosophila, which is often called the "common fruit fly". Nearly 5,000 described species of tephritid fruit fly are categorized in almost 500 genera of the Tephritidae. Description, recategorization, and genetic analyses are constantly changing the taxonomy of this family. To distinguish them from the Drosophilidae, the Tephritidae are sometimes called peacock flies, in reference to their elaborate and colorful markings. The name comes from the Greek τεφρος, tephros, meaning "ash grey". They are found in all the biogeographic realms.

<span class="mw-page-title-main">Ephydroidea</span> Superfamily of flies

The Ephydroidea are a superfamily of muscomorph flies, with over 6,000 species.

<i>Ceratitis capitata</i> Species of insect

Ceratitis capitata, commonly known as the Mediterranean fruit fly or medfly, is a yellow-and-brown fly native to sub-Saharan Africa. It has no near relatives in the Western Hemisphere and is considered to be one of the most destructive fruit pests in the world. There have been occasional medfly infestations in California, Florida, and Texas that require extensive eradication efforts to prevent the fly from establishing itself in the United States.

<span class="mw-page-title-main">Parasitoid wasp</span> Group of wasps

Parasitoid wasps are a large group of hymenopteran superfamilies, with all but the wood wasps (Orussoidea) being in the wasp-waisted Apocrita. As parasitoids, they lay their eggs on or in the bodies of other arthropods, sooner or later causing the death of these hosts. Different species specialise in hosts from different insect orders, most often Lepidoptera, though some select beetles, flies, or bugs; the spider wasps (Pompilidae) exclusively attack spiders.

<span class="mw-page-title-main">Genetically modified insect</span> Insect that has been genetically modified

A genetically modified (GM) insect is an insect that has been genetically modified, either through mutagenesis, or more precise processes of transgenesis, or cisgenesis. Motivations for using GM insects include biological research purposes and genetic pest management. Genetic pest management capitalizes on recent advances in biotechnology and the growing repertoire of sequenced genomes in order to control pest populations, including insects. Insect genomes can be found in genetic databases such as NCBI, and databases more specific to insects such as FlyBase, VectorBase, and BeetleBase. There is an ongoing initiative started in 2011 to sequence the genomes of 5,000 insects and other arthropods called the i5k. Some Lepidoptera have been genetically modified in nature by the wasp bracovirus.

<i>Anastrepha ludens</i> Species of fly

Anastrepha ludens, the Mexican fruit fly or Mexfly, is a species of fly of the Anastrepha genus in the Tephritidae family. It is closely related to the Caribbean fruit fly Anastrepha suspensa, and the papaya fruit fly Anastrepha curvicauda.

<i>Zaprionus</i> Genus of flies

The genus Zaprionus belongs to the family fruit fly Drosophilidae and is positioned within the paraphyletic genus Drosophila. All species are easily recognized by the white longitudinal stripes across the head and thorax. The genus is subdivided in two subgenera, based on the presence of an even or odd number of white stripes. The species of the genus can be found in Africa and Southern Asia. One species, Zaprionus indianus, has invaded the New World.

<i>Drosophila hydei</i> Species of fly

Drosophila hydei (mosca casera) is a species of Diptera, or the order of flies, in the family Drosophilidae. It is a species in the hydei species subgroup, a group in the repleta species group. Bizarrely, it is also known for having approximately 23 mm long sperm, 10 times the length of the male's body. Drosophila hydei are commonly found on compost piles worldwide, and can be rudimentarily identified by eye owing to their large size and variegated pigment pattern on the thorax. The name derives from Dr R. R. Hyde, who first discovered that the species was distinct from Drosophila repleta. D. hydei are one of the more popular flies used as feeders in the pet trade. A few varieties are available, some flightless. They are very similar to Drosophila melanogaster, despite having separated 50 million years ago.

<i>Anastrepha suspensa</i> Species of fly

Anastrepha suspensa, known as the Caribbean fruit fly, the Greater Antillean fruit fly, guava fruit fly, or the Caribfly, is a species of tephritid fruit fly. As the names suggest, these flies feed on and develop in a variety of fruits, primarily in the Caribbean. They mainly infest mature to overripe fruits. While thought to have originated in Cuba, the Caribbean fruit fly can now also be found in Florida, Hispaniola, and Puerto Rico.

<i>Leptopilina</i> Genus of wasps

Leptopilina is a genus of parasitoid wasp in the family Figitidae. The genus is best known for the three Drosophila parasitoids Leptopilina boulardi, Leptopilina heterotoma and Leptopilina clavipes, used to study host-parasite immune interactions. The venom released by L. heterotoma during oviposition contains virus-like particles that delay host larval development and suppress the host cellular immune response. There is no evidence that these virus-like particles are the products of viral DNA as described in other parasitoid taxa.

<i>Scaptomyza flava</i> Species of fly

Scaptomyza flava is an herbivorous leaf mining fly species in the family Drosophilidae. In Latin, flava means golden or yellow. The fly is amber to dark brown in color and approximately 2.5 mm in length. In Europe and New Zealand the larvae are pests of plants in the order Brassicales, including arugula, brassicas, broccoli, Brussels sprouts, bok choy, cabbage, canola, cauliflower, horseradish, kale, kohlrabi, napa cabbage, nasturtium, radish, rapini, rutabaga, turnip, wasabi and watercress. In New Zealand, its range has expanded to include host species that are intercropped with salad brassicas, including gypsophila, otherwise known as baby's breath, which is in the pink family (Caryophyllaceae) and the pea in the Fabaceae. More typically, S. flava is oligophagous within the Brassicales. Scaptomyza are unusual within the Drospophilidae because the group includes species that are truly herbivorous. Other herbivorous drosophilids include D. suzukii, which attacks fruit very early during ripening and species within the genus Lordiphosa, from Africa and Asia, which also include leaf miners. Most drosophilids feed on microbes associated with decaying vegetation and sap fluxes.

<i>Drosophila quinaria</i> species group Species group of the subgenus Drosophila

The Drosophila quinaria species group is a speciose lineage of mushroom-feeding flies studied for their specialist ecology, their parasites, population genetics, and the evolution of immune systems. Quinaria species are part of the Drosophila subgenus.

<i>Drosophila silvestris</i> Species of fly

Drosophila silvestris is a large species of fly in the family Drosophilidae that are primarily black with yellow spots. As a rare species of fruit fly endemic to Hawaii, the fly often experiences reproductive isolation. Despite barriers in nature, D. silvestris is able to breed with D. heteroneura to create hybrid flies in the laboratory.

<i>Zaprionus tuberculatus</i> Species of fly

Zaprionus tuberculatus is a member of the subgenus and genus Zaprionus, family Drosophilidae, and order Diptera. It is an invasive fruit fly that originated in Africa, but can also be found in Europe and Asia. The fly earned its common name, the "vinegar fly", because researchers frequently captured the species using vinegar traps. Z. tuberculatus was previously considered a strictly tropical fly, but evidence of invasion to nontropical regions such as Turkey has been shown.

Hawaiian <i>Drosophila</i> Group of flies

The Hawaiian Drosophilidae are a lineage of flies within the genus Drosophila. This monophyletic clade includes all of the endemic Hawaiian Drosophila and all members of the genus Scaptomyza, which contains both Hawaiian and non-Hawaiian species. The Hawaiian Drosophilidae are descended from a common ancestor estimated to have lived 25 million years ago. Species of Hawaiian Drosophilidae flies have been studied as models of speciation and behavioral evolution. Along with other members of the native Hawaiian ecosystem, the conservations status of many species of Hawaiian Drosophilidae is threatened by habitat loss and introduced predators, among other factors.

Drosophila ochrobasis is an endangered species of fly from Hawaii, in the species rich lineage of Hawaiian Drosophilidae. It is found on the Big island of Hawaii, and has historically been recorded from four of the five volcanoes, though it is now largely absent from most of those sites. This species is in the adiastola subgroup and is closely related to D. setosimentum, but male D. ochrobasis have strikingly different wing markings.

References

  1. ↑ Matsumura, S. (1931). 6000 illustrated insects of Japan-Empire (in Japanese). Tokyo, Japan: Toko Shoin. pp. 1689 [367].
  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.; Zalom, Frank G. (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 . S2CID   86098875.
  3. 1 2 3 4 5 6 Kanzawa, T. 1939 Report. Translated from Japanese by Shinji Kawaii
  4. 1 2 3 4 5 6 7 Walsh, D. Press Release, Washington State University. 2009 Archived August 6, 2010, at the Wayback Machine
  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.{{cite journal}}: Cite journal requires |journal= (help)
  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 Archived 2016-04-30 at the Wayback Machine
  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. Bibcode:2020NatSR..1015358F. doi:10.1038/s41598-020-72074-8. PMC   7506528 . PMID   32958797.
  9. 1 2 3 4 5 6 7 8 9 10 11 12 13 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.
  10. ↑ Ometto, Lino; Cestaro, Alessandro; Ramasamy, Sukanya; Grassi, Alberto; Revadi, Santosh; Siozios, Stefanos; Moretto, Marco; Fontana, Paolo; Varotto, Claudio; Pisani, Davide; Dekker, Teun; Wrobel, Nicola; Viola, Roberto; Pertot, Ilaria; Cavalieri, Duccio; Blaxter, Mark; Anfora, Gianfranco; Rota-Stabelli, Omar (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. PMC   3641628 . PMID   23501831.
  11. 1 2 3 4 5 6 Poland, Therese M.; Patel-Weynand, Toral; Finch, Deborah M.; Miniat, Chelcy Ford; Hayes, Deborah C.; Lopez, Vanessa M., eds. (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" (PDF). Washington Invasive Species Council . 2017. 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 Archived 2010-03-28 at the Wayback Machine
  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" (PDF). Louisiana Department of Agriculture and Forestry. August 2010. Archived from the original (PDF) on 2011-01-12. Retrieved 2011-01-18.
  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". MSU Fruit Crop Advisory Team Alert. 29 Oct 2010. Archived from the original on 2011-07-20. Retrieved 2010-10-29.
  19. ↑ Hamilton, K. Wisconsin Pest Bulletin. 19 November 2010
  20. ↑ "Spotted Wing Drosophila IPM Working Group". NortheastIPM.org. 2012-11-13. Retrieved 2019-11-19.
  21. ↑ "Spotted Wing Drosophila | Minnesota Department of Agriculture". www.mda.state.mn.us. Retrieved 2019-11-19.
  22. ↑ Belgian Journal of Zoology - Drosophila suzukii (Diptera: Drosophilidae): A pest species new to Belgium. - Link Archived 2022-03-30 at the Wayback Machine
  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 Archived 2010-08-01 at the Wayback Machine
  24. ↑ "USDA Awards $6.7 Million To Stifle Spotted Wing Drosophila". Growing Produce. 2015-10-20. Retrieved 2019-11-19.
  25. ↑ "Monitoring | Cornell Fruit Resources". fruit.cornell.edu. Retrieved 2019-11-14.
  26. ↑ "Spotted wing drosophila in home gardens". extension.umn.edu. Retrieved 2019-11-14.
  27. ↑ "Spotted Wing Drosophila Management Guidelines--UC IPM". ipm.ucanr.edu. Retrieved 2019-11-14.
  28. ↑ Dam, Doriane; Molitor, Daniel; Beyer, Marco (2019). "Natural compounds for controlling Drosophila suzukii". Agronomy for Sustainable Development. 39 (6). doi: 10.1007/s13593-019-0593-z . S2CID   207987437.
  29. ↑ "New guide to organic management of spotted wing Drosophila released". Organic Agriculture. 19 June 2018. Retrieved 2019-11-14.
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  31. ↑ "SWD-killing wasps to make their debut". Good Fruit Grower. 23 November 2020. Retrieved 2020-12-05.
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  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. Bibcode:2012ApEnM..78.4869H. doi:10.1128/aem.00841-12. ISSN   0099-2240. PMC   3416361 . PMID   22582060.
  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. S2CID   84245460.
  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 . PMC   4592600 . 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. PMC   5847158 . PMID   29568251.

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