Harmful Diptera Pests in Garlic and Onion and Their Management

Abstract

Garlic (Allium sativum) is a hardy perennial member of the onion family presumably native to Central Asia; however, it has long been naturalized in southern Europe and throughout the world. Onion, on the other hand, is used all over the world, and its consumption depends mostly on the income level of consumers. It is an indispensable vegetable in the kitchen of many homes. Onions take third place in vegetable production after potato and tomato in Turkey. Mites, nematodes, and insect species cause damage to these plants, reducing considerably their yield. Among these pests, the most destructive are Delia platura Meigen (Diptera: Anthomyiidae) and Delia antiqua Meigen (Diptera: Anthomyiidae). The crop losses can sometimes reach up to 100%, depending on the crop and density of the pest. There are different methods to control these pests that vary by the pest type and the crop being applied. D. platura eat the contents of newly planted seeds, leaving empty seed shells and preventing germination. Also, D. antiqua. Young onions are particularly vulnerable. When the hide and bulb become entangled in the damaged plant, development stops, the plant turns yellow, and it breaks. Both pests are controlled using biological and chemical methods.

1. Introduction

Garlic (Allium sativum) is a hardy perennial onion family member most likely native to Central Asia, but it has been adopted in southern Europe and many other cuisines. It is one of the oldest cultivated vegetables used for its edible parts and as traditional medicine. As it is with onions, garlic is not used alone in cooking. It is one of the indispensable vegetables of the kitchens due to its taste and flavoring properties. Garlic teeth and leaves have appetizing, diuretic, antibacterial, respiratory and digestive tract antiseptic, and antithyroid effects. In addition, garlic has the properties of purifying bile, lowering blood sugar and lipids, cough suppressant, blood pressure lowering, anti-infective, and curative [1].

Onion is used all over the world, and its consumption depends mostly on the income level of consumers. It is an indispensable vegetable in the kitchen of many homes giving flavor and taste to the dishes. It regulates metabolism and strengthens the immune system against microbial diseases. It is known as a beneficial food for breastfeeding mothers due to its stimulating milk-production properties. In addition, onion is recommended to be included in the nutrition programs for children growth as it is an important energy source and a medicinal plant whose use dates back to ancient years [2].

There are different methods to control these pests that vary by the pest type and the crop being applied. Delia antiqua Meigen (Diptera: Anthomyiidae), Delia platura Meigen (Diptera: Anthomyiidae), Thrips tabaci L. (Thysanoptera: Thripidae), Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), Rhyzoglyphus spp., (Acari: Acaridae), Tyrophagus spp. (Acari: Acaridae), Aceria tulipae (Keifer) (Acari: Eriophyoidea) reduce the production of garlic. Previous studies carried out in Turkey reported garlic pests as Bactericera tremblayi Wagner (Hemiptera: Psylloidea), T. tabaci, F. occidentalis (Thysanoptera: Thripidae), Acrolepiopsis assectella (Zeller) (Lepidoptera: Acrolepiidae), Agriotes spp. (Coleoptera: Elateridae), Liriomyza spp. (Diptera: Agromyzidae), and Ditylenchus dipsaci (Kühn) (Tylenchida: Anguinidae) in garlic cultivation areas [3]. However, in recent years, garlic producers have complained about side effects of the pest on garlic production. The pests have been common and caused significant loss of garlic yield. Some producers have even maintained that they did not get any yields. The most important of these are D. antiqua Meigen (Diptera: Anthomyiidae and D. platura Meigen (Diptera: Anthomyiidae). Product loss as high as 35% on average is caused when no control is applied. The crop loss may sometimes reach up to 100%, depending on the crop and density of the pests. There are different pest control methods that vary by pest type. Besides chemical control for D. platura and D. antiqua, environmentally friendly practices such as yellow sticky traps are utilized for successful control of the Diptera pests [4].

2. Harmful Diptera species in garlic and onion

2.1 Seedcorn maggots (D. platura)

Seedcorn maggot or the bean seed fly, D. platura is a small dipterous insect. This fly is almost identical to the cabbage maggot (Delia radicum) and onion maggot (D. antiqua). In previous studies, this fly was named Hylemia platura, Hylemia cana, Hylemia cilicrura, and Hylemia similis [5]. Although D. platura was first reported in Germany, it is now spread all over the world [6].

The adult is about 6 mm long, gray in color, its body is covered with black hairs, and the wings are held crossed on the abdomen at rest. The egg is white in color, 0.6–0.7 mm long, and 0.2 mm wide. The larva is ivory-colored, thin on the front, wide on the back, and 5–6 mm in length. Pupa is barrel-shaped (Figure 1a–d).

Figure 1.

Delia platura, (a) adult (wikipedia), (b) egg (Kilic, T), (c) pupae (Kilic, T.), (d) larva, (Erdogan, P), (e, f) damage (Erdogan, P).

There is no mandatory diapause. After the adult emerges from the pupa, it feeds on flowers and other sweet substances and lays its eggs for 10–18 days. Usually, seedcorn is found in newly plowed and irrigated fields. D. platura lays its eggs singly or in groups. It also lays eggs on degraded organic material in soil cracks and especially in manure piles. The hatched larvae immediately go under the soil and begin to feed on organic materials. Meanwhile, the larva searches for germinating seeds in seed beds and quarries. It feeds on the stems and cotyledons of young seedlings. Total larval development time is 8–11 days depending on temperature. D. platura has three larval stages. When the larva completes its development, it leaves the plant it feeds on and becomes a pupa at a depth of 5–6 cm in the soil. Pupation period is 10 days at 20°C. A female lays 40–50 eggs in her lifetime. Male flies live 20–25 days, while females live 30–35 days. The development period from egg to adult is 35 days at 10°C and 16–17 days at 25°C. D. platura produces 3–4 generations per year [7].

The seedcorn maggot is a polyphagous pest that attacks over 40 different host plants [8]. Allium species have been reported to host D. platura [9, 10]. The larvae feed by opening galleries in the stems and newly formed cotyledons of seeds germinating in seed beds or quarries such as squash, melon, cucumber, beans, garlic, and other vegetables [11]. When the seedling emerges from the soil, only the cotyledons attract attention because the shoot tip is eaten. During the seedling stage, plants turn yellow, and dry. D. platura is the most destructive in garlic. Seedcorn maggots, according to Bessin [12], damage newly planted seeds by feeding on seed contents, often leaving empty seed shells and preventing germination (Figure 1e and f). Seedlings that germinate despite the damage are spindly and have few leaves, and they die before maturing. Seedcorn maggots can sometimes be found tunneling within stems and germinating seeds [13]. Early planting dates, heavy cover crops, and cool-wet weather all contribute to seedcorn maggot damage [12]. D. platura also feeds in garlic. D. platura is the most harmful species in garlic fields, and it was spread throughout the entire area with the rate of harmful infestation increasing to 41% in some areas in Turkey [14]. In Ecuador, seedling losses of more than 60% have been reported 2 weeks after sowing. Plants that survive are weaker and less resistant to subsequent pest and pathogen attacks [15].

2.1.1 Management

2.1.1.1 Cultural control

• Planting in highly organic soils, wet soils, or during wet weather periods should be avoided as much as possible, as this frequently leads to increased risks.

• Manure should be allowed to age and be thoroughly incorporated into the soil before using.

• During seeding, dragging a chain behind the planter removes the seed row moisture gradient, which attracts oviposition by adult flies. This practice reduces seedcorn maggot damage significantly.

• Sanitation practices such as removing flowering weeds from outlying areas to eliminate nearby food sources for adult flies and removing sweet-smelling substances reduce an area’s attractiveness to these flies.

• There have been isolated reports of spider and bird predation on adults, as well as fungus diseases on larvae. However, none of these predators are thought to be effective at controlling seedcorn maggot populations.

• Because they spend so much of their life underground, seedcorn maggots do not appear to have many natural enemies [16].

Kessing and Mau [11] suggested reusing manure and thoroughly incorporating it into the soil before planting. Planting when the soil and weather conditions favor rapid germination is a preventive measure against seed corn maggot infestation. According to Basin [12] planting, shallow planting, higher seeding rates, a well-prepared seedbed, and turning the cover early are all preventative measures for seed corn maggots (which renders the field less attractive to egg laying by flies). In another study, it was discovered that no-till fields are less likely to have seedcorn maggot problems because germinating seeds alone do not attract large populations of egg-laying females [17].

2.1.1.2 Biological control

Seedcorn maggots do not appear to have many natural enemies because they spend much of their life cycle underground. Isolated incidences of predation by spiders, ants, and birds upon adults and of fungal diseases infecting larvae have been reported, but none of these predators or pathogens is considered significant in controlling the population of seedcorn maggots [16]. There are some studies on the biological control of D. platura. Ellis and Scatcherd [4] revealed that two nematode parasitic species, Steinernema feltiae and S. krausseri, can be used to control seed fly and onion fly. The same study determined that S. feltiae reduced numbers of bean seed fly larvae by about 50%. Moreover, onion seedlings treated with the entomopathogenic fungus Beauveria bassiana (strain ANT-03) based insecticides were less attacked by the pest [18]. Recently, entomopathogenic nematodes (EPNs) have been proposed as a potential control method for Delia species [19, 20].

2.1.1.3 Chemical control

In problematic areas, seed spraying should be performed or seed beds should be sprayed before planting seeds. If seedlings are infected after planting, spraying should be done to prevent new contamination [11]. Before planting, the seeds should be sprayed with drugs containing active substances Imidacloprid, Thiamethoxam, and Acetamiprid. If there is a need to spray during the green period, a chemical pesticide containing cyromazine as active ingredient can be applied.

2.2 Onion fly (Delia antiqua)

Onion maggot, D. antiqua, is a major underground agricultural pest, found throughout Asia, Europe, and North America due to its high and low temperature tolerance [21, 22].

Adult of D. antiqua is similar to adult houseflies but slightly smaller. The adult is 6 mm long and gray in color. There are five dark bands on the thorax of the adults. Wings of adults are transparent and unblemished; legs and antennae are black. D. antiqua eggs are matte, white in color, 1.5 mm long, and banana-shaped. There are 12 longitudinal lines on the egg [23]. Larva is white and legless. The head of the body is narrow and shaped like a carrot that widens toward the end. Mature larva is 6–8 mm. D. antiqua pupae are reddish, 6 mm long, and barrel-shaped (Figure 2a–d).

Figure 2.

Delia antiqua, (a) adult (Pest and diseases image library, (b) egg (Pest and diseases image library), (c) larva (Rasbak), (d) pupa (Rasbak), (e, f) damage (wikipedia.org).

Adults begin to appear in mid-March and early April, depending on climatic conditions. Adults emerge gradually throughout the following month. Temperature affects the length of the preoviposition period. Flies kept at 25°C laid eggs in 10–24 days, with a 15-day average. Adults lay their eggs in groups of 10–20 or singly, usually in the place where they meet with the onion, on leaves, tuber bark, and cracks in the soil, within 10–20 days following emergence. Flies in captivity lay up to 123 eggs at the rate of 1–45 per day. Eggs hatch in 3–6 days, depending on temperature and proportional humidity. The emerging larvae enter from the junction of the onion and the beet and move toward the inside of the onion. The larval period is 15–20 days. The mature larvae pupate in the soil near the onion plant [24]. The pupal period is 10–15 days. In addition to the damage it causes by feeding on the plant tissue, the larva causes decay with various bacteria it carries. The damage is especially greater in young onions. In the damaged plant, the development stops, the plant turns yellow, and it breaks when the hide and bulb are caught. Since the shallots that come out of the onion seeds planted for the purpose of growing shallots are frequent, the damage is more common (Figure 2e and f) [25]. The seed value of shallots is lost, and they rot. Onions, garlic, and bulbous flowers are their hosts [26, 27].

2.2.1 Management

2.2.1.1 Cultural control

There are numerous non-chemical approaches to D. antiqua management. Crop rotation, crop sanitation, delayed planting, protective barrier installation, biological control, and sterile insect technique are examples of these.

• Crop rotation can considerably reduce damage by D. antiqua.

• Crop sanitation, including the removal of cull and volunteer onions, proper disposal of culls and volunteers, and avoiding damaging bulbs in the field is an important facet of D. antiqua management.

• Delayed planting can help as D. antiqua flies preferentially oviposit on larger onions.

• While onion plant varieties show little susceptibility to D. antiqua, garlic varieties have greater sensitivity.

• Since D. antiqua oviposits on or at the base of onion plants, the use of physical barriers to exclude flies has been considered; row covers effectively reduce infestations of both D. platura [28, 29, 30, 31].

2.2.1.2 Biological control

Pests of Delia spp. are vulnerable to a variety of natural enemies and biocontrol agents. Many (60–100) species of staphylinid and carabid ground beetles, generalists that feed on eggs and early instars, prey on Delia spp. [32]. In addition to feeding on eggs, some staphylinid beetles, such as Aleochara bilineata Gyllenhal (Figure 3a) and A. bipustulata Linnaeus, parasitize Delia pupae [32]. Aphaereta pallipes Say (Figure 3b) is a braconid fly, which has a diverse host range and successfully parasitizes D. antiqua. Moreover, other biocontrol agents of Delia include predators and parasitoids as well as entomopathogenic fungi (EPFs) and nematodes (EPNs). Entomophthora muscae (Figure 3c), Metarhizium anisopliae (Figure 3d), and B. bassiana (Figure 3e) have all been found to be capable of infecting and killing Delia sp. pests in EPF screenings [33, 34, 35]. Similarly, EPNs, including commercially (Nemaplus, Biotem, Larvanem, Capsanem, etc.) available species such as S. feltiae (Figure 3f) and Heterorhabditis bacteriophora (Figure 3g) infect D. antiqua [36].

Figure 3.

(a) Aphaereta pallipes, (b) Aleochara bilineata, (c) Entomophthora muscae, (d) Metarhizium anispliae, (e) Beauveria bassiana, (f) Steinernema feltiae, (g) Heterorhabditis bacteriophora (wikipedia.org).

2.2.1.3 Sterile insect technique

Sterile insect technique (SIT) is a pest management technique that involves rearing and sterilizing large numbers of a pest before releasing them into the wild population. Sterile males compete with fertile males for the opportunity to mate with fertile females, reducing the number of viable offspring [37].

2.2.1.4 Chemical management

Growers rely heavily on chemical management tactics due to the practical and economic limitations of non-chemical management tools. Currently, Delia antiqua is managed principally with insecticides applied as seed treatments and in-furrow applications of chlorpyrifos at planting [38]. Because flies move and disperse during the day, sprays targeting flies are unlikely to contact the pest and are not recommended for fly management, although some growers continue to use them [29].

2.3 Leaf miners (Liriomyza spp.)

Adults are 1–2 mm long, gray-black in color. Larvae are up to 3 mm, white yellow in color, and clear (Figure 4a–d). Adults are on all leaves of the plant, and larvae are gallery life miner adults and live 25–30 days. A female lays about 400 eggs between two epidermises of the leaf. Larvae that emerge from egg feed by opening various galleries in the leaf epidermis. The mature larva, which has completed its development, leaves itself the soil to become pupae [39].

Figure 4.

Liriomyza spp. (a) Adult, (b) egg, (c) larva, (d) pupa (Payne J.A.), (e, f) damage (wikivand.com).

The females inflict small wounds on leaves, feed on the sap that comes out of it, and cause cell disruption. Feeding causes loss of healthy leaf tissue, so that plant cannot capture enough sunlight and often becomes infected with disease. Plants often fail to grow or produce crops. Then damaged areas turn yellow and dry and the leaves fall (Figure 4e and f). They delay development in young plants and seedlings. They cause quality and yield loss. They are harmful to tomatoes, eggplant, peppers, beans, peas, broad beans, lettuce, zucchini, cucumbers, spinach, onions, and leeks [39].

2.3.1 Management

2.3.1.1 Cultural control

• The soil is plowed at a depth of 10 cm, and the pupae in the soil are destroyed.

• Contaminated plant waste should be disposed.

2.3.1.2 Biotechnical control

It can be used as yellow sticky traps to control adults of Liriomyza spp.

3. Conclusions

Garlic and onion foods have been known for their health benefits since ancient times and are frequently used for both health promotion and flavor purposes. The positive effects of garlic and onion also called a natural antibiotic among people are innumerable, and new benefits continue to be discovered every day. Both play a huge role in the health of people, such as reducing the risk of various types of cancer, improving mood, and maintaining skin and hair health. There are many pests that limit the production of these plants. For example, D. platura, Delia antiqua, Liriomyza spp., and Ditylenchus dipsaci. Especially, D. platura, D. antiqua cause a high rate of product loss when these two pests are not controlled. In order to prevent product loss caused by D. platura and D. antiqua, correct control methods must be applied. Onion and garlic farmers should be informed about these pests and their control.