Distribution. Onion maggot is found throughout the northern hemisphere, and apparently it was introduced to North America from Europe soon after European colonists arrived. It was recognized as a pest in the New England states by the early 1800s, and reached western onion-growing regions by the early 1900s. Onion maggot now is distributed widely in the United States and southern Canada. However, it apparently is absent from Florida in the southeast, and Arizona and New Mexico in the southwest. It is considered a serious pest only in northern areas.
Host Plants. Onion maggot attacks plants in the family Alliaceae (Amaryllidaceae). Onion is the principal host, but chive, garlic, leek, and shallot are sometimes attacked. Wild onion apparently is not a suitable host. It is possible to rear onion maggot larvae on abnormal hosts such as radish and turnip (Workman, 1958), but adults normally do not deposit eggs on such plants. (See color figure 33).
Onion maggot adults are particularly attracted to decaying onions, such as those infected with the soft-rotting bacteria Erwinia carotovora or Fusarium fungus
(Dindonis and Miller, 1980). Survival may be slightly higher, or development time shorter, for onion maggot larvae feeding on microbe-infected onions (Zurlini and Robinson, 1978). Older onion maggot larvae are usually fully capable of attacking and developing satisfactorily on disease-free onions (Schneider et al., 1983). However, survival of young maggots is poor on mature onions unless they are wounded or infected with disease. Indeed, survival of the third generation of onion maggots is likely dependent on the availability of unhealthy onions.
Natural Enemies. Numerous insects are known, or suspected, to prey on onion maggots. Tomlin et al. (1985) provided a comprehensive list of natural enemies from Ontario that was likely a representative of the predator and parasitoid complex in North America. Parasitoids included Aleochara bilineata (Gyllen-hal), A. bipustulata (Linnaeus), A. curtula (Goeze) (all Coleoptera: Staphylinidae); Aphaereta pallipes (Say) (Hymenoptera: Braconidae); Spalangia rugosicollis Latreille and Sphegigaster sp. (both Hymenoptera: Pter-omalidae). Among the common predators were mites (Acari), rove beetles (Coleoptera: Staphylinidae), his-ter beetles (Coleoptera: Histeridae), sap beetles (Coleoptera: Nitidulidae), ground beetles (Coleoptera: Carabidae), and ants (Hymenoptera: Formicidae). Eggs and larvae were much more susceptible to predation than pupae, probably because of their smaller size. The authors concluded that the parasitoids Aleochara bilineata and Aphaereta pallipes, which caused 21% and 17% mortality, respectively, were among the most important mortality agents. Predation is much more difficult to measure, so the relative importance of predators is less certain. However, such predators as Bembidion quadrimculatum L. (Coleoptera: Carabidae) were reported to consume 25 onion maggot eggs per day (Grafius and Warner, 1989), so predators surely have an important role in onion maggot population biology. Aleochara bilineata is unusual in that though larvae parasitize the pupal stage of onion maggot, the adults feed on maggot eggs and young larvae (Royer et al, 1998; Royer and Boivin, 1999).
The fungus Entomophthora muscae commonly infects onion maggot and many other flies. Dead, spore-covered flies are often found attached to elevated portions of plants following fungus outbreaks. Carruthers et al. (1985) conducted a study of this fungus in Michigan, and concluded that while abiotic factors such as humidity and temperature likely were important in disease cycle development, host and pathogen densities were more critical factors. Flies contact fungus, and become infected, both on host-plant foliage and in the soil. Death of adults occurs in 7-9 days after exposure to conidia (Tu and Harris, 1988). The soil is the principal overwintering reservoir for the fungus. The spring and autumn generations of onion maggot exhibited higher levels of infection.
Life Cycle and Description. The number of generations is two, or more commonly three, per year— with a proportion of each generation diapausing as puparia until the next year. In Quebec, adults from overwintering insects appear in May and initiate the first generation (Lafrance and Perron, 1959; Boivin and Benoit, 1987). Peak emergence of the first generation occurs in early July. The second generation begins emerging in mid- to late-August, with peak emergence about the first of September. Third generation insects all enter diapause, forming the overwintering population that emerges the following spring. The proportion of insects entering diapause in the first and second generations is reported to be about 25% and 60%, respectively. During exceptionally warm summers fewer insects enter diapause. Very similar patterns of emergence were observed in Pennsylvania (Eyer, 1922), and Oregon (Workman, 1958).
The biology of onion maggot was given by Eyer (1922), Workman (1958), and Perron (1972). Methods of onion maggot rearing were provided by Allen and Askew (1970) and Blaine and McEwen (1984). Effect of radiation on onion maggot was given by McEwen et al. (1984). An interesting account of Delia ecology, and implications for management from a British perspective, was found in Finch (1989).
Onion maggots can be extremely damaging in northern onion producing areas. In New York, for example, 40-80% losses are realized regularly if insecticides are not used (Martinson et al., 1989). Damage to onions often occurs in early to mid-summer; the damage that occurred earlier in the development of the onion plant is more often due to seedcorn maggot,
which may be active as early as April (Miles, 1955b). When onion maggot larvae feed on relatively small onions they may completely hollow out the young bulb, causing rapid death. A single onion maggot larva may kill several seedling onions, whereas as the onions grow larger the larvae are not compelled to disperse to other onions to find food. Later in the season the onions are more tolerant of onion maggot feeding, and there may not be above-ground signs of maggot feeding, but the bulbs can incur additional damage from secondary invaders such as soil-borne fungi and seedcorn maggot. Onions nearing maturity are most susceptible to these secondary organisms. Twelve-week-old onions are not very suitable for survival of onion maggots (Finch et al., 1986) unless they are mechanically damaged or infected with disease. Mechanical damage to bulbs during harvesting can lead to attack by third generation flies of bulbs drying in the field (Eckenrode and Nyrop, 1986). Carruthers et al. (1984) have developed procedures for estimating plant damage.
There appears to be a close relationship between onion maggot and soft rot of onion caused by Erwinia carotovora. The maggot creates wounds where the bacterium can enter the onion. The surface of several stages of the insect may be contaminated with the bacterium, thus aiding dispersal. Also, the bacterium is found in the puparium, which provides protection and allows survival during inclement periods. The insect also benefits from this relationship, because onion tissue infected with soft rot bacteria are more suitable for development of larvae. The relationship is not entirely specific, however, and several other flies such as seedcorn maggot, and several otitidids (Diptera: Otitidae), are attracted to rotting onions (Harrison et al., 1980).
Sampling. Onion maggot flies use both olfactory and visual cues to find their host plant. This information has been exploited to develop sampling techniques. Flies will orientate up-wind in response to onion volatiles (Judd and Borden, 1989), and various trap designs employing inverted cones suspended above onion bulbs or baited with the onion chemical n-dipropyl disulfide have been devised to capture adults (Dindonis and Miller, 1980). Enzymatic yeast hydrolysate is also attractive (Miller and Haarer, 1981). Yellow traps also are recommended for capture of onion maggot flies, and sometimes yellow-sticky traps are baited with onions. Vernon et al. (1989), however, reported that white traps were more effective. Traps capture more flies when they are positioned within 20-30 cm of the bare soil. The adults prefer to land on horizontal surfaces. Therefore, water pan traps are more appropriate than vertical sticky traps (Finch and Collier, 1989).
Heat-unit accumulations have been used to predict developmental rates of onion maggot (Boivin and Benoit, 1987) and as an aid to estimating optimal timing of insecticide applications (Eckenrode et al., 1975). Careful timing of adult control reduced the number of insecticide treatments from 7-12 annually to only two, with excellent results (Liu et al., 1982). Phenological development of plants also serves as an indicator of fly flights (Boivin and Benoit, 1987).
Insecticides. In many areas, insecticides are routinely used to protect against damage by onion maggot. Application of granular or liquid insecticide formulations to the furrow at planting, or over the row after planting, are common. Treatment of seed with insecticides is also beneficial, but some materials are phyto-toxic when applied in this manner (Saynor and Hill, 1977). Disruption of first generation onion maggot helps protect against damage by later generations even if the insecticide residue has dissipated (Ritcey et al., 1991). However, long-lasting insecticides are more effective, and in the absence of these, adult suppression is practiced to protect against second- and third-generation onion maggots (Finch et al., 1986). Insecticide applications to foliage are common, but in many areas insecticides are also applied to the harvested bulbs drying in windrows. To avoid illegal insecticide residues on onions, it is important to use insecticides that are not very persistent for treatment of dry bulbs (Frank et al., 1982). Insecticide resistance is common in many onion-growing areas (Harris and Svec, 1976; Straub and Davis, 1978; Harris et al., 1982; Hayden and Grafius, 1990).
Biological Control. Several fungi, including Beau-veria bassiana and Paecilomyces fumosoroseus, have been evaluated for suppression of onion maggot, but the puparia and adults seem to be relatively insensitive (Majchrowicz et al., 1990).
Cultural Practices. The only significant host of onion maggots is onions, and usually commercially produced crops of onions. Therefore, crop rotation is sometimes a suggested component of pest management. The potential for onion maggots to cause damage is directly related to the previous presence of onions (Martinson et al., 1988). However, onion maggots disperse randomly over distances that exceed 2 km (Martinson et al., 1989), so it is difficult to achieve adequate isolation.
Sanitation is an important component of onion maggot management. Damaged bulbs left in the field are an important food source for overwintering populations, much more so than are cull piles and volunteer onions (Finch and Eckenrode, 1985). Volunteer onions are, in fact, highly attractive to ovipositing flies in the spring, but few maggots survive on these plants. This suggests the possibility of using early-planted trap crops to lure females from the principal crop. Miller and Cowles (1990) suggested use of a combination of cull onions as an oviposition attractant, and application of a chemical oviposition deterrent to onion seedlings, to minimize damage. Efforts should be made to minimize damage to bulbs when tilling, or at harvest, as these injured bulbs are very suitable for onion maggot larval development. If onion culls are to be disked in the autumn, it is best to wait until third generation flies have oviposited, as this deprives flies of additional suitable oviposition sites.
Soil conditions influence onion maggot, but the relationship of soil to population biology warrants additional research. Egg hatching and larval survival are higher in moist soil. Only if larvae are exposed to saturated soil for protracted periods will high soil moisture levels be a problem. Perron (1972) reported that sites with heavy soil, rich in clay, were less suitable for onion maggot than the sites with organic soil. Onion maggots apparently prefer to oviposit on organic soils, and abundance of beneficial insects is higher in organic soils.
Crop density may affect onion maggot damage. Perron (1972) reported that high onion densities were beneficial, principally due to dilution of onion maggot injury over more onions. Parasite activity was also enhanced in high density plots.
In New York, Walters and Eckenrode (1996) demonstrated the benefit of several approaches to onion maggot suppression. Crop rotation in combination with partially resistant onion varieties and decreased rates of insecticide were effective in preventing damage.
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