American Serpentine Leafminer Liriomyza trifolii Burgess Diptera Agromyzidae

Natural History

Distribution. This native leafminer has long been found throughout the eastern United States and Canada, northern South America, and the Caribbean. In recent years it has been introduced into California, Europe, and elsewhere, resulting in a fairly cosmopolitan distribution. There is increasing international traffic in horticultural crops, particularly flowers, which is thought to be the basis for the expanding range of this species. Liriomyza trifolii readily infests greenhouses, so range expansion seems likely to continue, including some northern climates. As a vegetable pest, however, its occurrence is limited principally to tropical and subtropical regions.

The taxonomy of this group was greatly confused until about 1980. Consequently, many records before this time are incorrect or unsubstantiated. Confusion with vegetable leafminer, L. sativae Blanchard, has been especially frequent.

Host Plants. Liriomyza trifolii is perhaps best known as a pest of chrysanthemums and celery, but it is highly polyphagous. For example, Stegmaier (1966b) reported 55 hosts from Florida, including bean, beet, carrot, celery, cucumber, eggplant, lettuce, melon, onion, pea, pepper, potato, squash, and tomato. Flower crops that are readily infested and which are known to facilitate spread of this pest include chrysanthemum, gerbera, gypsophila, and marigold, but there are likely many other hosts, especially among the Compositae. Numerous broad-leaved weed species support larval growth. Schuster et al. (1991) found that the nightshade Solanum americanum; Spanish needles, Bidens alba; and pilewort, Erechtites hieracifolia; were suitable weed hosts in Florida. (See color figure 7.)

Natural Enemies. In North America, parasitic wasps of the families Braconidae, Eulophidae, and Pteromalidae are important in natural control, and in the absence of insecticides, they usually keep this insect at low levels of abundance. At least 14 parasi-toid species are known from Florida alone. Species of Eulophidae such as Diglyphus begina (Ashmead), D. intermedius (Girault), D. pulchripes, and Chrysocharis parksi Crawford are generally dominant in most American studies, though their relative importance varies geographically and temporally (Minkenberg and van Lenteren, 1986). Many of the parasitoids attacking L. trifolii also attack L. sativae.

Predators and diseases are not considered to be important, relative to parasitoids. However, both larvae and adults are susceptible to predation by a wide variety of general predators, particularly ants.

Life Cycle and Description. Leafminers have a relatively short life cycle. The time required for a complete life cycle in warm environments such as California and Florida is often 21-28 days, so numerous generations can occur annually in tropical climates. Leibee (1984) determined growth at a constant 25°C, and reported that about 19 days were required from oviposition to emergence of the adult. Development rates increase with temperature up to about 30°C; temperatures above 30°C are usually unfavorable and larvae experience high mortality. Minkenberg (1988) indicated that at 25°C, the egg stage required 2.7 days for development. The three active larval instars required 1.4, 1.4, and 1.8 days, respectively. The time spent in the puparium was 9.3 days. Also, there was an adult preovipostion period that averaged 1.3 days. The temperature threshold for development of the various stages is 6-10°C except that egg laying requires about 12°C. (The American serpentine leafminer adult in color figure 176 is referred to on page 198.)

  1. The eggs are deposited in the middle or lower stratum of plant foliage. The adult seems to avoid immature leaves. The female deposits the eggs from the lower surface of the leaf, but they are inserted just below the epidermis. Eggs are oval in shape and small in size, measuring about 1.0 mm long and 0.2 mm wide. Initially they are clear but soon become creamy white.
  2. Body length and mouth parts can be used to differentiate instars; the latter is particularly useful. For instar one, the mean and range of body and mouth parts (cephalopharyngeal skeleton) lengths are 0.39 (0.33-0.53) mm and 0.10 (0.08-0.11) mm, respectively. For instar two, the body and mouth parts measurements are 1.00 (0.55-1.21) mm and 0.17 (0.150.18) mm, respectively. For instar three, the body and mouth parts measurements are 1.99 (1.26-2.62) mm and 0.25 (0.22-0.31) mm, respectively. A fourth instar occurs between puparium formation and pupation; this is a nonfeeding stage and is usually ignored by authors (Parrella, 1987). The puparium is initially golden brown, but turns darker brown with time.
  3. The adults are small, measuring less than 2 mm long, with a wing length of 1.25-1.9 mm. The head is yellow with red eyes. The thorax and abdomen are mostly grey and black though the ventral surface and legs are yellow. The wings are transparent. Key characters that serve to differentiate this species from vegetable leafminer, Liriomyza sativae Blanchard, are the matte, greyish-black mesonotum and the yellow hind margins of the eyes. In vegetable leafminer the mesonotum is shining black and the hind margin of the eyes is black. The small size of this species serves to distinguish it from pea leafminer, Liriomyza huidobrensis (Blanchard), which has a wing length of 1.7-2.25 mm. Also, the yellow femora of American serpentine leafminer help to separate it from pea leafmi-ner, which has darker femora. (See color figure 176.)

Adult longevity is 13-18 days. Leibee (1984), working with celery as a host plant, estimated that oviposi-tion occurred at a rate of 35-39 eggs per day, for a total fecundity of 200-400 eggs. Parella et al. (1983) reported similar egg production rates on tomato, but lower total fecundity, because tomato is a less suitable larval host. The female makes numerous punctures of the leaf mesophyll with her ovipositor, and uses these punctures for feeding and egg laying. The proportion of punctures receiving an egg is about 25% in chrysanthemum and celery, both favored hosts, but only about 10% in tomato, which is less suitable for larval survival and adult longevity. Although the female apparently feeds on the exuding sap at all wounds, she spends less time feeding on unfavorable hosts. Adults are weak fliers, and often are blown by the wind. Males live only 2-3 days, possibly because they cannot puncture foliage and therefore feed less than females, whereas females usually survive for about a week. Typically, they feed and oviposit during much of the daylight hours, but especially near mid-day.

A good summary of American serpentine leafmi-ner biology was published by Minkenberg and van Lenteren (1986). Keys for the identification of agromy-zid leafminers could be found in Spencer and Steyskal (1986).

Damage

The numerous punctures caused by females during the feeding and oviposition processes can result in a stippled appearance on foliage, especially at the leaf apex and margins. However, the principal form of damage is the mining of leaves by larvae, which results in destruction of leaf mesophyll. The mine becomes noticeable about 3-4 days after oviposition and becomes larger in size as the larva matures. The pattern of mining is irregular. Both leaf mining and stippling can greatly depress the level of photosynthesis in plant tissue (Parrella et al., 1985). Extensive mining may cause premature leaf drop, which can result in lack of shading and sun scalding of fruit. Wounding also allows entry of bacterial and fungal diseases.

There is some disagreement about the relative importance of leaf mining, and many studies have had difficulty in demonstrating an adverse effect of leaf mines on yield. Varieties and cultural practices undoubtedly contribute to some of the inconsistency observed, but clearly crops such as tomatoes are quite resilient, capable of withstanding considerable leaf damage. It is often necessary to have an average of 13 mines per tomato leaf before yield reductions occur (Levins et al., 1975; Schuster et al., 1976). In potatoes, Wolfenbarger (1954) reported sizable yield increases with as little as 25% reduction in leafminer numbers,

Adult American serpentine leafminer.

but leafminers were considered less damaging than green peach aphid, Myzus persicae (Sulzer).

Management

  1. Various techniques have been evaluated to assess larval and adult population densities. Counting mines in leaves is a good index of past activity, but many mines may be vacant. Counting live larvae in mines is time consuming, but more indicative of future damage. Puparia can be collected by placing trays beneath foliage to capture larvae as they evacuate mines, and the captures are highly correlated with the number of active miners (Johnson et al., 1980). The adults can be captured by using adhesive applied to yellow cards or stakes. Sequential sampling plans for determining the need for treatment, based on the number of mined leaves, were developed by Wolfenbarger and Wolfenbarger (1966). Zehnder and Trumble (1985) developed similar plans based on counts of puparia and flies.
  2. Chemical insecticides have long been used to protect foliage from injury, but insecticide resistance is a major problem. Insecticide susceptibility varies widely among populations, and level of susceptibility is directly related to frequency of insecticide application (Mason et al., 1989). In Florida, for example, longevity of insecticide effectiveness is often about 2-4 years, and then is usually followed by severe resistance among the treated populations. Rotation among classes of insecticides is recommended to delay development of resistance. Reduction in dose level and frequency of insecticide application, as well as preservation of the susceptible genotype through nontreat-ment of some areas, are suggested as means to preserve insecticide susceptibility among leafminer populations (Mason et al., 1989). Insect growth regulators can be more stable, but are not immune from the resistance problem. Neem is sometimes reported to be effective for leafminer suppression (Jyani et al., 1995).

Some insecticides are highly disruptive to naturally occurring biological control agents, particularly para-sitoids. Use of many chemical insecticides exacerbates leafminer problems by inducing extremely high leaf-miner populations. This usually results when insecticides are applied for lepidopterous insects, and use of more selective pest control materials such as Bacillus thuringiensis is recommended as it allows survival of the leafminer parasitoids.

Biological Control. Because parasitoids often provide effective suppression of leafminers in the field when disruptive insectides are not used, there has been interest in release of parasitoids into crops. This occurs principally in greenhouse-grown crops, but is also applicable to field conditions. Parrella et al.

(1989) published information on mass rearing Digly-phus begini for inoculative release. Steinernema nematodes have also been evaluated for suppression of leaf-mining activity. One of the most complete studies, by Hara et al. (1993), showed that high levels of relative humidity (at least 92%) were needed to attain even moderately high (greater than 65%) levels of parasitism. Adjuvants that enhance nematode survival increase levels of leafminer mortality (Broadbent and Olthof, 1995).

Cultural Practices. Because broadleaf weeds and senescent crops may serve as sources of inoculum, destruction of weeds and deep plowing of crop residues is recommended. The adults experience difficulty in emerging from anything but a shallow layer of soil.

Cultural practices such as mulching and staking of vegetables may influence both leafminers and their natural enemies. Price and Poe (1976) reported that leafminer numbers were higher when tomatoes were grown with plastic mulch or tied to stakes. At least part of the reason seems to be due to lower parasitoid activity in plots where tomatoes were staked. However, whereas Wolfenbarger and Moore (1968) reported that aluminum mulch seemed to repel leaf-miners in tomato and squash plantings, Webb and Smith (1973) found this not to be the case.

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