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Control of Drosophila suzukii by entomopathogens

Since a few years, the Drosophila suzukii has been a real nuisance in the European vineyards. Healthy ripening grapes fall prey en masse, resulting in harvest losses and major economic damage. Fighting the Drosophila suzukii is difficult, but entomopathogens – nematodes, bacteria, fungi and viruses that are specifically pathogenic to insects – may offer a solution.

The Drosophila suzukii (also called the Asian fruit fly or the spotted wing drosophila) was first seen in Europe in 2008 in Spain and Italy, and was in 2012 already spread throughout the whole of Northwest Europe. Drosophila suzukii, unlike the most common native European fruit fly – the Drosophila melanogaster – causes a lot of damage to the vineyards. This is because the Drosophila suzukii females are able to prick through the thin skin of (almost) ripe intact grapes with their much longer ovipositor to lay eggs. The Drosophila melanogaster cannot do this and only lays eggs in already broken or decaying fruit and therefore causes a lot less damage1-3.

Drosophila Suzukii female with magnified ovipositor
Drosophila Suzukii female with magnified ovipositor. Note: only the male flies have spots on their wings.
Martin Cooper via CC BY 2.0

The Drosophila suzukii can be controlled with insecticides (Spinosad / Tracer)4, but these – due to the risk of remaining residues on the grapes – cannot be used in the last moment of the ripening phase, or are toxic to beneficial insects such as bees. The fruit flies therefore have free rein at the most crucial moment of the season. It is possible to hang nets, or even to put each bunch in a separate bag, but this is costly and labor intensive. A lot of research is therefore being done on biological and ecological agents that can be used until late in the ripening phase. Natural enemies and entomopathogens of the Drosophila suzukii therefore receive full attention.

The following paragraphs will briefly discuss which natural enemies and entomopathogens (nematodes, bacteria, fungi and viruses) are known for the Drosophila suzukii, and how effective they are in killing the fruit flies.

Natural enemies

Many natural enemies have been tested – including Hemiptera (such as aphids, heteroptera and cicadas), beetles and mites – in the control of the Drosophila suzukii. In a closed lab environment these had a limited effect, but this effect was no longer observable in the field5. The only natural enemy that did have an effect on the development of the Drosophila population was the parasitic wasp. There are different types of parasitic wasps, and they all lay their eggs in a Drosophila larva or pupa. The larva still develops into a pupa, but in all cases the pupa is then eaten by the larva of the wasp. Native European parasitic wasps can parasitize more than 50% of the Drosophila melanogaster larvae, but are not able to parasitize larvae of the Drosophila suzukii. Wasps that originate from the natural habitat of the Drosophila suzukii, such as the Asobara japonica and the Asobara leveri, are better able to parasitize the larvae. One wasp has been found, the Asobara sp. TK1, that parasitizes specifically the larvae of the Drosophila suzukii. However, these wasps have only been tested under lab conditions and can produce completely different results in the field. In addition, it is not very desirable to introduce very exotic wasps from China or Japan into the European vineyards. Two European wasps, that parasitize not the larvae but the pupae of the Drosophila, the Pachycrepoideus vindemmia and the Trichopria drosophilae, show very good results in the lab (up to 90% parasitized pupae)6,7. The release of Trichopria drosophilae in an orchard shows that they can ensure a reduction of the amount of Drosophila suzukii. However, the results are not yet so successful that it can immediately be used on a large scale in viticulture8.

Parasitic wasp (Ceraphron sp. F)
Parasitic wasp (Ceraphron sp. F)
Pierre Bornand via CC BY-NC 2.0

Nematodes

Nematodes are small roundworms that live in the soil or in (the digestive tract of) other organisms. Crops such as grapevines can be sprayed with water to which nematodes have been added9. The Steinernema kraussei, Steinernema carpocapsae, Steinernema feltiae and Heterorhabditis bacteriophora nematodes are capable of killing at least 50, 80, 80 and 95% of Drosophila suzukii larvae, respectively. The Steinernema Kraussei nematode is the least efficient in killing larvae, but compensates for this by achieving the highest mortality rate in the pupae with 55%. The other three nematodes cause approximately 40% of the Drosophila suzukii pupae to die10. The three Steinernema nematodes have also been previously tested for blueberries, but then had no effect on the development of the Drosophila suzukii11. On the other hand, when applied to strawberries, and in particular the Steinernema feltiae, the nematodes do decrease the number of adult Drosophila suzukii (up to 35%)REF12. These differences in the effectiveness of the nematodes may be due to the differences in the test set-up tested, such as the amount of nematodes used, or the type of crop on which it was tested. All these nematodes are freely available on the market9 and there is very little legislation or regulation associated with the use of nematodes. They are “completely safe for humans, the environment, the crop and other natural enemies”13. But this is not entirely correct, the nematodes can kill the larvae and pupae of various insects that not all have to be harmful to the grapes. Apart from this, there are also nematodes that feed on the roots of the vine and thus cause root rot and loss of yield14. However, the entomopathogenic nematodes mentioned above do not damage the roots, but only parasitize insects. Therefore, nematodes have the potential to combat the Drosophila suzukii, but good field tests are needed to determine their actual efficiency (and damage to other insects).

Nematodes from the pupa of a wax moth
Nematodes from the pupa of a wax moth
USDA Agricultural Research Service via Public Domain

Bacteria

Only two entomopathogenic bacteria are known to have an effect on the development of Drosophila suzukii. The first is the Bacillus thuringiensis that can cause 44% mortality of the larvae, although this effect is highly dependent on the bacterial strain. The only Bacillus thuringiensis strain that actually causes death also produces the toxic protein β-exotoxin. This protein possibly explains the toxic effect, but is also toxic for vertebrates, which means that this bacterial strain is not suitable as a pesticide15. The other bacterium, Photorhabdus luminescens, has more potency and lives in symbiosis with the aforementioned nematode Heterorhabditis bacteriophora. This bacterium lives in the intestines of the ringworm and is released to the blood when the nematode has infected the fruit fly. Photorhabdus will produce enzymes and “toxin complexes” in the blood that break down the fly’s body into nutrients for the nematode and the bacterium itself. Photorhabdus luminescens –even at very low concentrations – effectively kills the larvae and pupae of the Drosophila suzukii (mortality of 70-100%)REF16. The Photorhabdus luminescens therefore seems very promising to prevent outbreak of a Drosophila suzukii pest. However, a disadvantage is that both the nematode and Photorhabdus luminescens are also toxic to other insects in the vineyard16.

There is already legal approval in Europe for the use of multiple bacterial strains in the vineyard. However, the majority of these bacteria are for use against botrytis and mildew. Of the above-mentioned bacteria against the Drosophila suzukii, there is only permission for a number of strains of the Bacillus thuringiensis. These bacterial strains are approved for use in the vineyard to combat the moths, the European grapevine moth (Lobesiabotrana) and the vine moth (Eupoecilia ambiguella), but are not approved for use against the Drosophila suzukii17.

Fun Fact: After the Battle of Shiloh during the American Civil War, the wounds of some soldiers began to illuminate and healed faster than expected. This “Angel’s glow” was probably caused by Photorhabdus luminescens. As its name implies, the bacterium is bioluminescent (it gives light). Moreover, it also produces an antibiotic to compete with other bacteria, and that came in handy for those wounded soldiers18,19.

Painting of the "Battle of Shiloh" by Thure de Thulstrup (1888)
Painting of the Battle of Shiloh – Thure de Thulstrup (1888).
Restoration by Adam Cuerden via CC BY 4.0

Fungi

The effect of entomopathogenic fungi on Drosophila suzukii larvae, pupae and adult flies is currently being fully tested. A number such as Beauveria bassiana, Isaria fumosorosea, Metarhizium anisopliae and Lecanicillium lecanii ensure a death rate of more than 50% among fruit flies11,20. The Metarhizium Brunneum fungus even causes a death of nearly 90% of fruit flies after ten days. In addition, it also reduces the fertility of the flies (during these ten days), resulting in fewer offspring20. The disadvantage of these fungi is that they can infect many other insects in addition to the fruit flies. The fungus Entomophthora muscae on the other hand is much more specific and will only have an effect on flies and mosquitoes. Unfortunately, this fungus causes a mortality rate of only 27% among the Drosophila suzukii21.

Although they are not always very specific to a particular insect, strains of many of these fungi have already been approved in Europe for use in crops such as strawberries or tomatoes. However, only use of Metarhizium anisopliae is permitted in the vineyard. The registration is only valid for use against phylloxera (Daktulosphaira Vitifoliae) and the black vine weevil (Otiorhynchus Sulcatus), but not against the Drosophila suzukii17. It should be noted here that the effects against Drosophila suzukii may be fungal strain specific11,20. Therefore, another strain of the same fungus that works against phylloxera does not necessarily have to be effective against the fruit fly (although this would be useful for obtaining European approval). So there are a number of fungi that achieve good results in the tests and are already registered in Europe for use with other crops and organisms. It would therefore be possible to use a number of these fungi to control the Drosophila suzukii within the foreseeable future.

Drosophila killed by Entomophthora muscae fungus
Drosophila killed by Entomophthora muscae fungus.
Adapted from Elya, 2017 via CC BY 4.0

Viruses

Viruses are often very specific to a specific organism and would therefore be a nice way to treat Drosophila suzukii specifically. Unfortunately, there are no known viruses that specifically attack the spotted wing drosophila. Several viruses are known to cause high mortality in the Drosophila melanogaster, but these viruses have little or no effect on the Drosophila suzukii. This is probably because the bacterium Wolbachia – that lives in symbiosis with Drosophila suzukii – prevents viral infections22.

The future

Since the emergence of the Drosophila suzukii in Europe, many new discoveries have been made regarding the natural control of this fruit fly. However, the disadvantage of all of the above natural enemies and entomopathogens is that they are often not very efficient, or are not specific to Drosophila suzukii. They can therefore also cause damage to other insects (or even vertebrates). Future studies should therefore show whether efficiency can be increased – for example, by combining a number of control methods – but also whether they can be used safely without causing serious damage to other ecosystems. A natural control does not always mean an ecologically responsible control! Some control methods are therefore very promising, but there is often still a long scientific and bureaucratic way to go before they can safely and effectively be used on a large scale in the vineyard.

Contact Koen Klemann, WineScience

References
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18.   Durham S. Students May Have Answer for Faster-Healing Civil War Wounds that Glowed 2001 [Available from: https://www.ars.usda.gov/news-events/news/research-news/2001/students-may-have-answer-for-faster-healing-civil-war-wounds-that-glowed/] Visited on 12-12-2018.
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