BIOLOGY OF LIRIOMYZA

Michael P. Parrella

Department of Entomology, University of California, Riverside, California 92521

PERSPECTIVES AND OVERVIEW

The genus Liriomyza, erected in 1894 (52), contains more than 300 species. They are distributed widely but are most commonly found in temperate areas; there are relatively few species in the tropics. Within this genus 23 species are economically important, causing damage to agricultural and ornamental plants by their leafmining activity (94). Many of these damaging species are polyphagous, which is uncommon among the Agromyzidae; of 2450 described species in this family only 11 are considered to be truly polyphagous, and 5 of these are in the genus Liriomyza (93).

“Serpentine leafminer” was proposed as a common name for any member of this genus because of the wide distribution, polyphagous nature, and morphological similarity of many of the species (98). The Entomological Society of America has adopted this naming policy, with a few exceptions (112). Indeed, many larvae of Liriomyza create serpentine mines, which are initially very narrow and gradually enlarge (57), often twisting through the leaf. However, the type of mine produced by Liriomyza may be influenced by the developmental stage of the leaf as well as by the host itself (99). Thus, the mines are not always serpentine in all host plants. In addition, mine location in leaves may vary considerably, and either the upper or lower leaf mesophyll may be mined (5, 71). Some species have larval stages that feed in potato tubers (50), bore through stems (34), and feed within seed heads (86).

Most of our knowledge concerning the biology of this genus comes from studies on economically important species. These data have been developed largely since 1900, with an explosion of information since 1975 (76). This reflects the dramatic rise of Liriomyza spp. as major pests of numerous ornamental and agricultural crops over the past ten years (72). As a result of this rise in economic importance, the proceedings from three formal conferences (80, 81, 87) and one informal conference (35) have been published. These, together with published reviews and bibliographies (38, 64, 76, 95, 95a), provide a good starting point for those interested in this genus. A comprehensive review of all economically important Agromyzidae (94) is an outstanding contribution to the biology, ecology, taxonomy, and control of these leafminers.

Out of necessity, this article contains general overviews of various biological parameters within this genus. Where specific studies have been done, these are cited~ It is intended that this article not be an exhaustive review of the literature, but rather a selective one covering those studies that best address specific biological aspects of the genus.

ADULTS

Emergence

Adults emerge through the dorsal anterior end of the puparium (the retained last larval integument within which pupation occurs) with the aid of the ptilinum (a temporary bladderlike inflatable structure). This process may take from 5 min to more than 1 hr. Some mortality may occur during this process (61). Newly emerged adults exhibit a positive phototactic response and climb up the sides of a cage or up the stalk of a plant, where they remain quiescent for a period of approximately 20 min while expanding their wings and body. The body is fully sclerotized and colored within 20 min-2 hr (16, 61). Adult females are usually larger than males and emerge from larger puparia (61, 65). Puparium size is positively correlated with adult vigor (65). Males appear to emerge prior to females (J. Yost & M. P. Parrella, unpublished); both sexes generally emerge during early morning hours (61). The time of day of peak emergence varies for different species (5). Studies of sex ratios of adults emerging from pupae indicate a 1:1 sex ratio (61, 96) or a slight

bias in favor of females (2, 5). Intensive laboratory rearing of L. trifolii over the past five years has produced approximately a 1:1 sex ratio of emerging adults (M. P. Parrella, unpublished).

Premating and Preoviposition

The majority of adults mate soon after emergence, and almost all females have mated within 24 hr (61, 69, 78). The period of time between adult emergence and mating, i.e. the premating interval, appears to be inversely related to temperature (16) and may differ for the sexes (96). The sexes may remain coupled for as little as 10 min (96), but the norm is 30 min-l hr. Maximum mating time is about 3 hr. Males and females mate more than once, and multiple matings by the female are needed for maximum egg production (61). Mating can usually be observed at any time of the day, but it generally occurs during early morning hours (16, 61).

It has been suggested that food, temperature, and relative humidity influence the preoviposition period (16), which may extend up to 5 days after adult emergence. Under greenhouse and laboratory conditions, most females begin oviposition within 24-48 hr after emergence (61, 78).

Mating

During copulation, the male assumes a position behind and alongside the female at about a 45° angle above her body. Occasionally, mounting from the front occurs. In the more typical position, the male’s forelegs clasp the mesothorax of the female, his middle legs clasp the female’s abdomen, and his hind legs spread the female’s wings. The wings of the male are held normally over the body. The male brings his abdomen forward and downward to connect to the female genitalia as the male’s hind legs move to rest on the substrate. This position is maintained throughout copulation (61; J. A. Bethke & M. P. Parrella, unpublished). No sex pheromone has been reported by researchers working with Liriomyza; however, it is possible that a stridulatory organ present in some males of Liriomyza spp. may be used in short-distance vocalizations to attract mates (95). Indeed, the rapid bobbing of males of L. trifolii when in close association with females may be a physical manifestation of this auditory signal (J. A. Bethke & M. P. Parrella, unpublished).

Aggressive behavior by male L. trifolii during mating has been observed in the laboratory under severely crowded conditions (J. A. Bethke & M. P. Parrella, unpublished). Upon the approach of a rival male, the coupled male will continually flex his wings until the intruder leaves.

Feeding and Oviposition Behavior

Excellent descriptions of leaf puncturing, feeding, and oviposition are available (7, 16, 61, 96, 111). The following description is from observations with L. trifolii (7), but similar behavior has been noted for L. sativae and L. huidobrensis (1. A. Bethke & M. P. Parrella, unpublished). When a female initiates a leafpuncturing sequence, the first event observed, regardless of host plant, is a bending of the abdomen to position the ovipositor perpendicular to the leaf. The ovipositor contacts the leaf through a series of rapid thrusts. Once the ovipositor has penetrated the leaf surface, the thrusts becomes slower and more deliberate. At this point the female damages mesophyll cells in a specific manner, creating one of two different types of leaf punctures. If the abdomen is twisted from side to side, a large fan-shaped leaf puncture is created. A tubular leaf puncture is produced when no abdominal twisting follows the puncture. Eggs are deposited in tubular leaf punctures. The difference between oviposition behavior and the creation of a tubular leaf puncture without an egg is subtle; oviposition entails a pause in slow thrusting followed by a final thrust to deposit an egg. After every leaf puncture the female backs over the wound and feeds from it. The female feeds from all punctures, regardless of whether or not they are used for oviposition. Hence, all leaf punctures can be considered feeding punctures (7); this should clarify considerable confusion in the literature. Males are unable to create their own punctures, but, as many authors indicate (56, 61), they feed from

punctures created by females. Leaf puncturing can reduce photosynthesis (71) and may kill young plants (17). Leaf puncture size varies with the size of the adult female (61).

Feeding and oviposition by adults appear to occur primarily during the morning, and the frequency of these activities is positively correlated with temperature (20, 66). Little adult activity is observed after 1800 hr (20, 61, 66, 78). Leaf puncturing may occur with equal frequency on the abaxial and adaxial leaf surfaces (69), but this may depend on the species.

Leaf puncturing and feeding by adult Liriomyza undoubtedly serves an important role in host plant assessment. It has been suggested (7) that host feeding is more important in this regard than leaf puncturing. Several researchers have examined the ratio of total punctures to oviposition punctures in an attempt to determine host plant suitability or a general biological characteristic of Liriomyza spp. (20, 61, 115). These ratios have ranged from 1:1 to 40:1 and vary with temperature (66), leaf quality, and host plant. Unless the leaf area exposed to flies (126) and the number of flies released onto the plant can be held constant, these ratios are of little value.

Egg-laying capacity varies considerably within the genus Liriomyza. Mean egg production per female ranges from less than 100 (25) to greater than 600 (61). Females generally lay the majority of eggs between days 4 and 10 of adult life, depending on temperature (48, 66, 69, 78). Fecundity is strongly related to food source and temperature (16, 61, 66, 78); maximum oviposition occurs between 20-27°C (16, 66) when a constant food source such as honey is provided. Unfertilized females oviposit hundreds of eggs that fail to develop, although ovarian development, egg laying, and other responses appear to be normal (61). Some fertilized females oviposit infertile eggs. Many studies report that individuals of certain Liriomyza spp. do not create feeding punctures or lay eggs (5, 61, 78).

Longevity

Most longevity studies have been conducted using caged flies in close association with a host plant or carbohydrate food source (16, 61, 66, 69, 78). Under these conditions, females live 15-20 days and males 10-15 days. Longevity generally decreases at higher temperatures; the presence of honey dramatically increases longevity. Although no studies have examined the longevity of these flies in the field because of the difficulty associated with studies on individual flies in nature, most laboratory studies have probably overestimated the normal longevity (as well as fecundity) of adults. In laboratory rearing studies (K. Heinz and M. P. Parrella, unpublished) we observed that increasing the size of the rearing container tended to shorten the longevity of L. trifolii. In addition, most longevity studies have not considered the importance of the times of adult emergence. For example, the deposition of eggs in leaf material during a 3-hr interval (e.g. during laboratory production) resulted in pupation over a 24-hr period and subsequent adult emergence over a 6-day span. When survivorship of adults emerging from these pupae was examined as cohorts based on the day of adult emergence, different survivorship profiles were produced (K. Heinz & M. P. Parrella, unpublished) (Figure 1). It is possible that a short larval development time may be correlated with adult vigor.

Adults are able to withstand freezing temperatures for short periods (62), 50 adults that emerge during warmer periods of winter in nearctic and palearctic regions may survive. Liriomyza trifolii, which is native to the southern part of the Nearctic, was considered incapable of overwintering in more northern areas. However, the survival of adults and pupae at low temperatures suggests that this species may be able to survive in these areas (53, 99). This factor and others may contribute to their colonization in these habitats.

The whitish, transluscent egg is deposited through the adaxial or abaxial leaf surface. The egg varies in size based on the size of the species: e.g. 0.25 mm x 0.10 mm for L. congesta (16) and 0.28 mm x 0.15 for L. huidobrensis (2). Liriomyza eggs may be confused with thrips eggs oviposited in leaf tissue (54). An eggstaining technique has been developed for detecting eggs of L. trifolii in celery, chrysanthemum, and tomato leaves (75). Eggs are laid singly, but often in close proximity to each other. No epideictic (ovipositiondeterring) pheromone [present in other Agromizidae (49)] has been discovered in Liriomyza (7). Egg nonviability has been estimated to be as high as 20% (5) and is dependent on temperature (16). The eggs

increase in size after oviposition, possibly through the imbibition of fluids from plant tissue (16, 102). The period of egg development varies with temperature and ranges from 2-8 days. There appears to be considerable variation in the relationship between temperature and development and in developmental threshold (6.2-13.4°C; Table 1), probably because of differences in species, host plants, and experimental methodology. Sixteen days at 1.1°C is required to cause 100% mortality of L. trifolii eggs in celery (42).

As the eggs develop they become opaque, and gradually the brownish cephalopharyngeal skeleton can be differentiated (5). When about to hatch, the larva is oriented with its anterior extremity, which contains the mouth-hook, at the terminus of the egg furthest from the original oviposition puncture made by the female (96). This position results from a 180° rotation of the embryo, whereby the anterior cephalic end moves toward the posterior end of the egg (5). In some species, the larva may eat the eggshell before moving into the leaf mesophyll (5) Pressure exerted by the larva causes the eggshell to become distended longitudinally and eventually to split at its anterior end.

LARVAE

The larva begins feeding immediately after eclosion and feeds incessantly until it is ready to emerge from the leaf (111). Different species of Liriomyza feed in different sections of the leaf mesophyll [e.g. L. trifolii in the palisade mesophyll, L. huidobrensis in the spongy mesophyll (71), and L. brassicae in the palisade and spongy mesophyll (94)]. Nonetheless, when larvae are forced to compete for resources because of crowding, they may tunnel into leaf stalks and into the main stem of the plant (96).

The larva is somewhat cylindrical and maggotlike. The anterior end tapers and the posterior end is truncate. Larvae move via peristaltic action of their hydrostatic skeleton. There are four molts and four larval instars. The fourth instar occurs between puparium formation and pupation and is rarely discussed by most authors. Black sclerotized mouthhooks are left within the mine after the molt and can be used to distinguish the duration of the instars (100), because there are distinct moutbhook sizes for each larval instar. Other researchers have used mine width as an indication of instar duration (109) Because interpretation may vary, the method used to determine larval instar duration must be known; unfortunately, many reports do not explain precisely how this was done. Because of the difficulty in separating larval instars, many authors combine all instars and simply refer to larval duration (Table 2). Authors commonly combine egg and larval development to examine the total F time of the immature stages spent within the leaf (see Table 4).

Larval development varies with temperature and host plant (Table 2). In addition, larval development time on a single host varies considerably with leaf position and age, but few authors take this into consideration. Many studies can also be criticized for lack of detail in explaining how development times were calculated (e.g. starting and stopping points, time of egg laying, sampling frequency). These points are especially critical for consistent calculations of the total larval duration of many Liriomyza spp., considering that it can be as short as 16 days at field/greenhouse temperatures (20, 41). Only one attempt to correlate laboratory development with the development of field populations has been reported (53); the development period for eggs and larvae in the laboratory, 147.5 day-degrees above 10. 1°C, corresponded well to the observed development in the field.

As the larvae develop, both the diameter of the mine and the rate of mine formation increase (20, 61). For L. trifolii, the volume of leaf material consumed by the third stage larva is 643 times greater than that consumed by the first stage larva, and the feeding rate is 50 times greater (20). Mining causes a reduction in leaf photosynthesis, with the amount of reduction varying according to mine location (71). Metabolic rates of larvae double for every 10°C increase in temperature, but the total amount of leaf tissue consumed by larvae apparently remains the same regardless of temperature (9).

Interspecific competition with mites and aphids may inhibit population increases of Liriomyza (59) by affecting larval development. Intraspecific competition in both the field and laboratory may reduce survivorship as well as size of larvae and pupae, and may thus reduce adult vigor (59, 65).

Figure 1. Percent emergence and survivorship of adult L. trifolii from 500 pupae. All emerged and pupated within a 24-hr period. Adults emerged over a 6-day period.

Table 1 Temperature-development studies with the egg stage of Liriomyza spp.

——————— Species of Liriomyza	———————————— Host	———————————— Development rate regressed on temperaturea	————————— Estimated threshold temperature for development (°C)	——————— Reference
——————— L. congestab	———————————— Vicia faba	———————————— y= 0.0355_x_+ 0.529	————————— 14.9	——————— (16)
L. sativaec	_Phaseolus_sp.	y= 0.0214_x_+ 0.133d	6.2	(62)
L. sativae	_Phaseolus_sp.	y= 0.0166_x_- 0.116	7.0	(109)
L. trifolii	Apium graveolens	y= 0.0343_x_- 0.441	12.8	(41)
L. trifolii	_Phaseolus_sp.	y= 0.0266_x_- 0.266	10.0	(13)
L. trifolii ———————	Chrysanthemum morifolium ————————————	y= 0.0261_x_- 0~352d ————————————	13.4 —————————	(13) ———————

a Simple linear regression with temperature ( x )(°C) = independent variable and development rate ( y ) (1/day) = dependent variable. The x -intercept method was used to calculate development thresholds.

b Reported as L. trifolii, but probably L. congesta (78).

c Reported as L. pictella, but probably L. sativae (94). d Upper temperatures not used in calculating the regression.

Table 2 Temperature-development studies with the larval stages of Liriomyza spp.

Species of Liriomyzaa ———————	Host ————————————	Developme regresse temperat ————————	nt rate d on urea —————	Estimated threshold temperature for development (°C) ————————	Reference ———————
L. congesta	Vicia faba	y= 0.0131_x_	- 0.165	12.6	(16)
L. sativae	_Phaseolus_sp.	y= 0.00657_x_	- 0.0305b	4.6	(109)
L. sativae	_Phaseolus_sp.	y= 0.0133_x_	- 0.105	7.9	(62)
L. trifolii	Apium graveolens	y= 0.007_x_	- 0.0587	8.4	(41)
L. trifolii	_Phaseolus_sp.	y= 0.0130_x_	- 0.111	8.5	(13)
L. trifolii	Chrysanthemum morifolium	y= 0.00509_x_	- 0.0313	6.1	(9)
L. trifolii ———————	Lycopersicon esculentum ————————————	y= 0.0118_x_ ————————	- 0.0926 —————	7.8 ————————	(91) ———————

a See footnotes on taxonomy and methodology, Table 1. b All development stages combined for regression analysis.

Table 3 Temperature-development studies with the pupal stage of Liriomyza spp.

Species of Liriomyzaa ———————	Host ————————————	Development rate regressed on Temmperaturea —————————————	Estimated threshold temperature for development (°C) ————————	Reference ———————
L. congesta	Vicia faba	y= 0.00662_x_- 0.0539	8.1	(16)
L. sativae	_Phaseolus_sp.	y= 0.00651_x_- 0.0631	9.7	(62)
L. trifolii	Apium graveolens	y= 0.00749_x_- 0.0771	10.3	(104)
L. trifolii	Apium graveolens	y= 0.00760_x_- 0.0779	10.3	(41)
L. trifolii	_Phaseolus_sp.	y= 0.00662_x_- 0.0529	8.0	(13)
L. trifolii	Chrysanthemum morifolium	y= 0.00600_x_- 0.0539	9.0	(77)
L. trifolii ———————	_Dendranthema_sp. ————————————	y= 0.00691_x_- 0.0771 —————————————	10.4 ————————	(53) ———————

a See footnotes on taxonomy and methodology. Table I. b Reperted as L. sativae, but probably L. trifolii.

Table 4 Temperature-development studies with various combined stages of Liriomyza app.

Species of Liriomyzaa	Life stages	Host	Development rate regressed on temperaturea	Estimated threshold temperature for development (°C)	Ref.
————— L. sativae	——————— Egg-adult	————————— _Phaseolus_sp.	——————————— y= 0.00381_x_- 0.0352	————————— 9.2	—————— (62)
L. sativae	Egg-pupa	_Phaseolus_sp.	y= 0.00310_x_- 0.0195	6.1	(109)
L. trifolii	Egg-adult	_Phaseolus_sp.	y= 0.00369_x_- 0.0311	8.4	(13)
L. trifolii	Egg-adult	Chrysanthemum morifolium	y= 0.00310_x_- 0.0195b	6.3	(13)
L. trifolii	Egg-adult	Apium graveolens	y= 0.00281_x_- 0.0229	8.1	(41)
L. trifolii	Egg-pupa	_Dendranthema_sp.	y= 0.00728_x_- 0.0786	10.1	(53)

a See footnotes on taxonomy and methodology, Table 1. b Upper temperatures not used in calculating the regression.

When the larva is ready to pupate it cuts a semicircular slit in the leaf surface, usually at or near the end of the mine. This slit may be located on the upper or lower leaf surface, but depends on the mining location of the larva within the mesophyll. The larva emerges with characteristic peristaltic locomotion. When it is three-fourths out of its mine, the anterior portion waves about high above the leaf surface and the larva literally falls out (61).

Movement outside the mine is the same as within and is accompanied by a rolling motion, which usually forces the larva to fall from the leaf to the ground. Larvae occasionally pupate on leaves or at the base of leaves, stems, or stalks, but this is more common on plants with large curled leaves (squash, gerbera, etc). Larvae emerge from leaves during early daylight hours (61), with the majority of emergence occurring before 0800 hr.

PREPUPAE AND PUPAE

The period between larval emergence and puparium formation is generally referred to as the prepupa. The prepupal period is about 2-4 hr (41, 61), but varies considerably with temperature. The prepupa is negatively phototactic and positively thigmotactic. This stage is extended when the prepupa is exposed to constant light in bare containers (62).

The duration of the pupal stage varies inversely with temperature (Table 3), but at least 50% of the total development time of a Liriomyza individual is spent in this stage. Total development time of the pupa at greenhouse/field temperatures is about 8-11 days. Estimated temperature thresholds for development are generally consistent for pupae (Table 3), unlike those for eggs and larvae. This is probably due to more standard estimation methods, because the pupae are exposed and easier to observe. Relative humidity between 30 and 70% is optimum for pupation. It has been suggested that the substrate in which pupation occurs influences successful development to the adult stage (62, 63). Pupal weight and development time and percent emergence of adults from pupae appear constant regardless of host plant (62, 128).

Pupae of L. trifolii have exhibited a diapause at 16°C in Italy (99). While this diapause has not been observed in Britain, pupae can remain viable outdoors for several months and are able to withstand freezing temperatures (53). Thus, outdoor populations of Liriomyza may survive long enough to reinfest subsequent glasshouse crops.

HOST-PLANT INTERACTIONS, MOVEMENT, AND DISPERSION

Adults

Because the larvae of Liriomyza are unable to leave one leaf and enter another, the ultimate choice of host selection rests with the ovipositing adult female. This fact has led to numerous studies of adult preference. Unfortunately, only those studies in which an effort was made to standardize the type, age, and size of the leaves offered to adult flies (126) are of value.

Adult females exhibit distinct preferences for host plants, although their feeding and oviposition behavior remains stereotypic regardless of host (7).

The distribution and density of plant trichomes, the phenolic content, and the nutritional value of hosts were found to influence host selection (19, 26, 36) Little quantitative data are available on withinplant preferences of egg-laying adults (3, 30, 88).

The basis for host-plant preference may be genetic. A comparison of laboratory-selected and wild populations of L. brassicae suggests an increased tendency to oviposit in the host that this species develops on (101).

Few studies on seasonal abundance and distribution of Liriomyza spp. have been performed in wild or agricultural systems where more than one species of plant or one species of Liriomyza may be present.

Research in this area has involved L. trifolii and L. sativae, which preferred celery and tomato, respectively (121, 122). There is evidence that L. trifolii may be replacing L. sativae in tomato (89) and gypsophila (83).

Liriomyza adults have long been known to be attracted to yellow cards, and with the application of adhesive these may be very effective monitoring tools (55) and may be useful in studies on movement and dispersal (31). Studies have confirmed that yellow is more attractive to adults than other colors (105), and that high reflectance through the yellow part of the spectrum increases catch (1, 11). Trap location with respect to the crop influences the number and species of flies captured (12, 123). The variance/mean relationship of L. trifolii and L. sativae trapped on yellow cards has been shown to be very consistent over time in chrysanthemum and tomato (70, 124).

An understanding of the movement and dispersal of economically important Liriomyza has been the objective of numerous studies over the past 35 years. In agricultural fields the within-field spread of leafminers begins slowly at first, generally originating in weed hosts in borders adjacent to field crops (22). Prevailing winds influence the rate and direction of dispersal from the center of origin. Densities are greatest at the point of origin and generally decrease with distance from the source (105, 116). In the greenhouse, where wind was not a factor, the mean distance flown by female flies (21.5 m) was greater than that flown by males (18.0 m) over a 7-day period (31). In addition, it was shown using a generalized distance dispersal model that density decreases more rapidly with distance for males than for females, and that males have slightly more aggregated distributions than females. Data on the sex ratio of adult Liriomyza caught on sticky yellow cards vary (12, 31), but most studies show capture of more males than females (11, 123). Based on the fact that females tend to live longer than males, one would expect that more females than males would be caught on yellow traps over a given period of time. Thus the data collected to date suggests differential attraction between the sexes.

The movement and dispersal of adults may be affected by aluminum-foil mulch around tomato and squash plants. This has been shown to reduce infestations of Liriomyza (119), presumably by repelling adult flies. Insecticides have also been shown to repel adults, although effectiveness varies with the chemical and method of application (85).

Larvae

In most cases, experimentally transplanted agromyzid larvae develop on plants phylogenetically related to their natural host and die on plants not related to the normal hosts (10). Some Liriomyza species, however, were successfully transferred among Compositae (Eupatorium sp.), Urticaceae (Cannabis sp.), and Labiatae (Galeopsis spp.). Larvae may be far less sensitive to repellent or deterrent chemicals than adults. This stage has evolved a completely parasitic mode of life within the plant; thus larvae have poorly developed sense organs, and hence little ability to discriminate among various host species (92). Consequently, if a female oviposits in plants outside its normal range, there is a possibility that the larva could complete development. This may offer one avenue of host-range expansion in Liriomyza

The possibility of sympatric genetic divergence in L. brassicae was investigated when genetic variation in survival and development time was demonstrated for three strains collected from different host-plant species (101). Formal quantitative genetic studies of L. sativae have been undertaken to determine the amount of genetic variation and to correlate this variation with parameters of host-plant utilization (107, 108). These techniques may be useful in the examination of host races in Liriomyza and other genera. A host race is defined as a group of individuals that genetically differs in host plant-related characters from individuals on other hosts. Individuals of the host race do not interbreed with individuals from other hosts because of divergent host preferences (107, 108). Genotype-environment interactions may be examined through correlations of various fitness components (e.g. development time) with environmental variables. These correlations provide estimates of local differentiation and the potential for future evolutionary change (108). Examination of L. sativae over a variety of adjacent crops revealed a significant genotype-environment interaction for development time within populations, which suggests that selection on individuals

residing on a crop could lead to host-plant specialization at the species level. The absence of host races in L. sativae has been attributed to frequent migration among closely spaced crops and to crop rotation (107). This promotes interbreeding and prevents groups from becoming isolated, which is necessary for the formation of races. Thus in the absence of agricultural manipulations or in large agricultural monocultures, host races may develop in Liriomyza (93). Monoculture may already have been responsible for the development of a host race in L. sativae isolated on melons (misidentified as L. pictella) (61, 94).

Most members of the Agromyzidae are homogametic (8). They generally have obscure polytene chromosomes, which may be why so few species have been studied cytologically (8). Only Liriomyza urophorina has been investigated (46, 47); it showed chromosomal polymorphism for six paracentric inversions.

In chrysanthemum, celery, and tomato the distribution of larvae and pupae from field samples is generally clumped (3, 30, 88, 124). When the variance/mean relationship is examined for larvae using Taylor’s power law, the a (a sampling factor) and b (a species-specific aggregation constant) values calculated for celery (3) and chrysanthemum (30) are very similar. This suggests that further work on celery may lead to sampling plans similar to those developed on chrysanthemum (30).

Leafminers respond favorably to high nitrogen content in leaves (23, 82, 120). Most of the data stem from studies in which nitrogen content is varied by manipulation of general fertilizer regimes. In many cases it is difficult to tell whether mines were fewer with lower fertilizer concentrations because of poor larval survival or reduced egg-laying by adults. A similar problem is encountered when one reviews the large body of information in which cultivars of one plant species are ranked as to sensitivity or resistance to leafminer damage (33, 90, 110).

ECONOMIC IMPORTANCE

The economic impact of Liriomyza leafminers in the United States and throughout the world has been considerable; in California alone it was estimated that the chrysanthemum industry lost approximately 93 million dollars to L. trifolii from 1981 through 1985 (57a).

Liriomyza leafminers can impact crops in at least six ways: (a) by vectoring disease (127), (b) by destroying young seedlings (17), (c) by causing reductions in crop yields (39, 117), (d) by accelerating leaf drop above developing tomatoes, thus causing “sunburning” of the fruit (26a), (e) by reducing the aesthetic value of ornamental plants (67), and (f) by causing some plant species to be quarantined (42, 54, 69, 72). While the results of most of these six types of damage are obvious [e.g. heavy mining and stippling in young seedlings or transplants can kill a plant and/or dramatically slow growth (17, 103)], it has been difficult to accurately associate specific levels of mining activity with reductions in crop yield. Reductions in photosynthesis and other physiological parameters have been measured in vegetable crops (29, 103) but have not been correlated to yield loss. Studies have shown that greenhouse-raised tomatoes can tolerate high levels of damage by L. sativae without suffering appreciable losses in yield (43). However, in a recent study (39), L. bryoniae on tomato caused yield loss, which was greatest when mining occurred in the leaves close to a young, developing fruit. Predetermined damage thresholds have been incorporated into sequential sampling plans for tomato (28, 114), but these plans have not received wide acceptance. An experimental threshold on L. sativae in southern coastal pole-tomato fields in California calls for treatment when an average of 10 pupae per sampling tray per day accumulate over a 31 day period (26a).

RESPONSE TO INSECTICIDES

Numerous articles have focused on chemical control of Liriomyza leafminers (76) because of their potential for causing damage. Control with insecticides is usually complicated by the insect’s biology, i.e. fast development time; smallness and high mobility of adults; a relatively long pupal stage occurring in the soil; high reproductive capability; and egg and larval stages within and protected by leaf tissue. In addition, a mine created by the larva remains in the leaf as long as the leaf survives; thus insecticide application may