“Alfalfa Blotch Leafminer”

(Figs 1–8)

Identification & Diagnosis. As in other Agromyza, A. frontella has one pair of prescutellar acrostichal setae (Fig. 2) and a stridulatory file on fused syntergites 1+2. It can be differentiated from congeners by having a costa that extends only slightly past vein R₄₊₅ (Fig. 3), at least 4 fronto-orbital setae, a reddish to yellowish frons that becomes more yellow anteriorly, and has the orbital plate and ocellar triangle dark, a reddish to yellowish parafacial, gena, scape and pedicel, a dark brown, long-haired male first flagellomere (Figs 1–3; only pubescent anterodorsally in female), 4 long, well-developed dorsocentral setae, a dark brown, lightly pruinose notum and a calypter with the margin and hairs dark. There are several spines along the surstylus, which is shallow and extensively fused to the epandrium (Fig. 5), and the apex of the phallus is divided into two short, cylindrical sections, the basal mesophallus and apical distiphallus, the latter of which is bent downwards and apically membranous (Figs 7, 8); the similar species A. drepanura Hering has the distiphallus straight, not bent downwards, the surstylus has 9–10 spines (not 4), and the venter of the mesophallus is produced as a narrower process (see Zlobin (2000: figs 4–8)). Wing length 1.6–2.2 mm. The larva has 8–12 pores on the anterior spiracle and 3 on the posterior spiracle.

Distribution. Agromyza frontella is relatively widespread in Europe and likely has a broad western to central Palaearctic distribution, with specimens also known from Afghanistan, Israel, Morocco and Tunisia (Spencer 1973; Zlobin 2000; Černý and Merz 2006; Loumerem et al. 2007; Martinez 2013).

It was introduced into eastern North America by at least 1968 when it was found in Massachusetts, and was soon thereafter detected in Ontario, Quebec and other Midwestern states, as discussed in Miller and Jensen (1970) and Venette et al. (1999). It is now known from much of northeastern North America from West Virginia and the Canadian Maritimes to Illinois, west to North Dakota and Alberta (Thompson 1974; Hendrickson and Barth 1978; Plummer and Byers 1981; MacCollom et al. 1982; Spencer and Steyskal 1986; Hutchison et al. 1997; Lundgren et al. 2003; Soroka and Otani 2011), although its actual distribution is likely much broader.

•Nearctic Region: Canada (Alberta Manitoba, New Brunswick, Nova Scotia, Ontario, PEI(?), Quebec, Saskatchewan), USA (Connecticut, Illinois, Massachusetts, Minnesota, New Jersey, New York, North Dakota, Ohio, Pennsylvania, Vermont, West Virginia, Wisconsin).

•Palaearctic Region: Afghanistan, Austria, Belarus, Czech Republic, Denmark, France, Germany, Hungary, Israel, Italy, Lithuania, Morocco, Netherlands, Norway, Poland, Russia, Slovakia, Spain, Sweden, Switzerland, Tunisia, Turkey, United Kingdom, former Yugoslavia.

Hosts. Agromyza frontella is a leafminer that most often occurs on Medicago L., including M. sativa falcata (L.) Arcang. (alfalfa) and M. lupulina L. (Spencer 1990), but it is also found on Melilotus Mill. and Trifolium L. (Benavent-Corai et al. 2005), all of which are Fabaceae species in the tribe Trifolieae.

Damage. If larval feeding is partial, leaflets are retained, but more extensive damage causes loss of leaflets and weakening of the plant (Hendrickson and Barth 1978).

Female feeding punctures, which may exceed 250 per leaflet and up to several thousand during the lifetime of the adult (Hendrickson and Barth 1978), also causes the leaf to become brittle, further reducing yield (Soroka and Otani 2011). Oviposition, larval activity and damage caused by female feeding punctures also aids in secondary infection by spring black stem - the fungal pathogen Ascochyta medicaginicola Qian Chen & L. Cai [as “Phoma medicaginis var. medicaginis Malbr. & Roum.” - see Richard and Guibord (1980)] - which causes black crown and root rotting in alfalfa (Rodriguez et al. 1990).

In Europe, this species infrequently causes appreciable damage, but it has been highly problematic in North America following its introduction, where alfalfa is widely grown as a forage crop. In North America, reductions in alfalfa yield have been estimated at 7–20%, and in some fields, over 70% of leaflets have been observed with larvae (Venette et al. 1999).

However, Daley and McNeill (1987) from work on alfalfa in Canada, found that overall forage accumulation and net photosynthesis did not differ between plots of uncontrolled and controlled (with insecticides) leafminers, even though the former were at higher densities.

Biology. This species has a life-cycle typical of leaf-mining agromyzids. Newly emerged females puncture leaflets to feed (Hendrickson and Barth 1978); larval survival is reduced in leaflets with high densities of punctures (Quiring and McNeil 1984a). In alfalfa, the larva is restricted to a single leaflet, where the full-depth mine is initially narrow and linear, following the leaf margin to the apex or sometimes the lateral margin, but then becomes blotch-like as the larva returns to the base via the mid rib (Dempewolf 2004). Many larvae can be found per leaflet and intraspecific competition and cannibalism among first instars is density dependent and results in lower survival rates (Quiring and McNeil 1984b). Pupation is in the soil (Spencer 1973). In Pennsylvania, USA, there are four generations per year (Plummer and Byers 1981).

Mellors and Helgesen (1978) in the USA found the highest immature stage survival at 20°C, but there was little difference in development rates between 20–25°C: the egg stage took 3.5–14 days; the larval stages 5.9–16.4 days; and the pupal stage 15.9–61.5 days. The photoperiod during egg and larval development influenced the initiation of pupal diapause; with a decrease in the light period from 18 to 10 h (tested at 15 and 20°C), diapause increased from less than 5% to greater than 55%. Temperature only affects diapause under a 14 h light period, where more pupae enter diapause if eggs and larvae are reared at 15°C than at 20°C (Therrien et al. 1985).

A female sex pheromone has been reported (Carrière et al. 1988) and there is evidence of an oviposition-deterring pheromone produced by females (McNeil and Quiring 1983).

Life table studies of field populations in the USA revealed that the most variable age-specific factors were oviposition and pupal survival of a current season: the former varying between 3–48% of potential oviposition, and the latter from 38–72% in non-diapausing populations. It is suggested that the variation in these factors results from the effects of alfalfa harvests on the environments of the adult and pupal stages (Mellors and Helgesen 1980).

Movement & Dispersal. No published information is available, but it is likely that this species shows behaviour typical of leaf mining agromyzids: thus, naturally capable of short distance flights. The transport of infested hosts would facilitate dispersal.

Management. Early detection. General information about this species is provided in a fact sheet produced by University of Wisconsin, Pest Management Program (University of Wisconsin 2016). For field monitoring, sampling plans for estimating the current egg and larval populations of the leafminer in alfalfa were developed in Canada, including the cost of sampling; recommendations include four leaves taken per stem and 200 stems per field (Hardcourt and Binns 1980a). Similar recommendations have been made for the estimation of mature larvae and pupae from soil: the former include the use of 40 pans to catch larvae per field; and the latter, 50 quadrats per field (Harcourt and Binns 1980b). Further to this, temperature-dependent models have been developed to predict the seasonal occurrence of the life stages to facilitate timely management to prevent population outbreaks in Eastern Ontario, Canada (Harcourt et al. 1983).

Control. Early cutting of alfalfa is recommended in Wisconsin, USA (University of Wisconsin 2016). Classical biological control (= introduction biological control) was undertaken in the USA and Canada. Fourteen hymenopterous parasitoids were introduced from Europe in the mid-late 1970s into Delaware, USA, with three species becoming established (Hendrickson and Barth 1979). Pre-parasitism levels before release was 18%, but two of the released species, Dacnusa dryas (Nixon) (Braconidae) and Chrysocharis punctifacies Delucchi, spread and increased parasitism levels to 72% by the early 1980s, causing leafminer density to fall below economic threshold levels (Drea and Hendrickson 1986; Hendickson and Plummer 1983). These two parasitoids were distributed to other states in the USA and also into Ontario, Canada in the late 1970s, where similar impacts were recorded (Heimpel and Meloche 2001).

“Barley Leaf Mining Fly”

(Figs 9–17)

Identification & Diagnosis. Similar to all other Agromyza, A. megalopsis has one pair of prescutellar setae and a stridulatory file on the lateral margin of abdominal syntergite 1+2 (Fig. 9). Also similar to other grass-feeding species of Agromyza, it is mostly brown (Figs 9–11), the male first flagellomere is slightly enlarged and apically haired and the mesophallus+distiphallus is capsule-like and sinuate (Figs 16, 17).

Unlike these other grass-feeders, this species is slightly more shining (Fig. 10), with some specimens almost indistinctly greenish (not green metallic as noted by Dempewolf (2004)), the antenna is black (not brown to dark brown), the parafacial and orbital plate are slightly raised, the costa ends only slightly past vein R₄₊₅ (not to M₁), the third dorsocentral is short but well-developed and a fourth and fifth are sometimes obvious, and the apical section of the distiphallus is slightly more elongate. Wing length is 2.5–2.7 mm. The posterior larval spiracles are closely adjoined and with 3 pores (Spencer 1973: fig. 356) – these spiracles are more widely spaced in the highly similar Agromyza nigrella (Rondani) (see Spencer (1973: fig. 6)).

Distribution. This species is known from the Palaearctic Region in much of Europe from Spain to Poland, Turkey and Uzbekistan, as well as Iraq and parts of northern Africa (Spencer 1973; Černý and Merz 2006; Martinez 2013), although is likely more widespread. The known distribution by country is as follows: Bulgaria, Cyprus, Czech Republic, Egypt, Greece (islands), France, Germany, Hungary, Iraq, Poland, Slovakia, Spain (Geigenmüller 1966), Turkey, Uzbekistan, former Yugoslavia.

Hosts. Agromyza megalopsis is a leafminer that likely attacks a number of different Poaceae, but so far it is known from barley (Hordeum vulgare L.), and possibly rye (Secale cereale) (Spencer 1973).

Damage. Agromyza megalopsis is considered the most significant Agromyza on cereals in Europe, sometimes co-occurring with other species during outbreaks (Dempewolf 2004). Mined leaves yellow, wilt and sometimes die. Although leaf damage does not always correspond to measurable drops in grain production, yield loss of 27% has been estimated in Bulgaria (Khristov 2000) and 20% in Germany (Spencer 1973).

Biology. Spencer (1973) and Dempewolf (2004) referred to studies on the biology of this species (Geigenmüller 1966; Scherney 1966; Weigand 1966; Scherney and Weigand 1967), which has sometimes been referred to incorrectly as A. nigrella.

Little recent information is available; most of the following is taken from Spencer (1973). Single females can lay 30–40 eggs. Oviposition is near the leaf base and 30–40 eggs have been recorded from a single leaf. Individual larvae create a narrow mine to the leaf apex, and then continue back towards the base as a broader, full-depth blotch mine; multiple larvae in one leaf result in merged mines (Ridland 2009). Pupation takes place in the mine but more commonly in the soil. In the former Czechoslovakia, sowing time and the use or absence of fertilizers did not affect the incidence of adults within winter and summer barley (Gallo 1989). In Europe, A. megalopsis completes one generation followed by a partial second generation each year; the latter overwinter as pupae (Khristov 2000; Spencer 1973).

Movement & Dispersal. No specific studies have been published but it is likely that the leafminer shows behaviour typical of leaf mining agromyzids; that is, naturally capable of short distance flights around and within a crop (Ridland 2009). Transport of cereals could facilitate dispersal (Ridland 2009).

Management. Early detection. A biosecurity plan for cereal leafminers (including A. megalopsis) has been prepared for the grains industry in Australia (Ridland 2009); this covers surveillance, basic biology and control measures to assist with preparedness should an incursion occur.

Control. Residues from crops should be removed and destroyed because leafminers can complete their life-cycle on cut plant material; deep ploughing is an alternative because adult emergence from puparia is reduced (Ridland 2009). In the Czech Republic, the use of the pyrethroid deltamethrin, together with liquid fertilizer on winter barley reduced leafminer populations (Kazda 1997). From a review of insecticide use, such as pyrethroids, carbomates and organophosphates, against agromyzids that attack cereals, Ridland (2009) also notes that these pests have not developed resistance in the same way that the polyphagous Liriomyza species have. However, the use of these chemicals may still have longer term negative effects; for example, by reducing parasitoid communities. Spencer (1973), summarizing earlier work, notes that high levels of parasitism from local hymenopterous parasitoids (chalcids and braconids) were reported from Germany in the 1960s. In Hungary, the parasitism rate of an overwintered population was 46%. The main parasitoid species was Chorebus Haliday sp. (Braconidae). Parasitized larvae remained in the leaf tissues (Darvas et al. 1984).

“Corn Blotch Leafminer”

(Figs 18–26)

Identification & Diagnosis. Similar to all other Agromyza, A. parvicornis has one pair of prescutellar setae (Fig. 19) and a stridulatory file on the lateral margin of abdominal syntergite 1+2 (Fig. 18). Also similar to other grass-feeding species of Agromyza, it is mostly brown, has only the two posterior dorsocentrals well-developed (remaining setae strongly reduced and sometimes inconspicuous), a slightly enlarged and apically haired male first flagellomere (Fig. 20), a costa that extends to vein M₁, and a characteristic phallus that has a capsule-like, sinuate mesophallus+distiphallus (Figs 23, 24). Agromyza parvicornis differs from the other grass-feeders in having the frons, at least the base of the first flagellomere and most of the gena orange-brown, the surstylus has over a dozen tubercle-like setae (Fig. 26), and the apical section of the distiphallus is laterally swollen and almost circular in appearance when viewed ventrally. Wing length is 2.5–3.2 mm. The posterior larval spiracles have 3 pores (Spencer 1973).

Distribution. Agromyza parvicornis is widespread in the United States and presumed to be present in most states (Frick 1959). In Canada, it is known from Quebec (Zhu et al. 2004), British Columbia and Ontario (Spencer 1969). Martinez and Etienne (2002) note its presence in the Neotropics in Argentina, Cuba, Guadeloupe, Puerto Rico, the Dominican Republic and Saint Vincent. Reported feeding of A. parvicornis on corn in Egypt by Zeinab et al. (1991) is likely a misidentification and requires verification.

Hosts. Agromyza parvicornis is a leafminer known from three species of Poaceae: Echinochloa crus-galli (L.) P. Beauv., Panicum miliaceum L. (millet) and Zea mays (corn). The presence of this species on Echinochloa P. Beauv. was considered a misidentification by Spencer (1969), and while he later re-listed it as a host (Spencer 1973), this association should be verified by further rearing.

Damage. In corn, larval feeding produces a broad blotch mine that may destroy a young leaf, but up to four larvae in a single developing leaf have been recorded (Spencer 1973) and many more can be found in a mature leaf. Feeding may consume all parenchyma, leaving only the epidermis behind, but in the tougher mature leaves only the lower parenchyma is touched (Spencer 1973; Wright 1998). The attacked leaf, depending on level of infestation, will dry and deform or shrivel, and sometimes die.

Spencer (1973) summarized some historical occurrences of outbreaks of Agromyza parvicornis, which are often small, isolated and produce moderate damage. However, instances of more considerable, severe destruction are known. Despite this, low to negligible loss of yield would be expected in corn, even given heavy feeding, unless combined with other biotic factors (Wright 1998) and poor growing conditions.

Biology. The following is taken from the summary of an earlier work by Spencer (1973), as no significant additional data have been published since that date. Oviposition occurs on the upper or lower surface of a young leaf, often apically, but eggs are laid anywhere on the leaf if mature. The development time of the larva is 10 or more days in the spring, but in the summer when temperatures increase, the time is only about four days. Pupation is external, just below the soil, and adult development takes about 14 days in summer months but several months in the winter.

In temperate regions, adults emerge by May and there are four generations per year. Further south, in Florida, adults emerge earlier (February) and some larval activity can continue through the winter.

Movement & Dispersal. No published information is available, but it is likely that this species shows behaviour typical of other leaf mining agromyzids, being capable of short distance flights. The transport of cereals and other hosts with leaves could facilitate dispersal.

Management. Early detection. General information about this species is provided in a fact sheet produced by the University of Florida, Cooperative Extension Service (Goyal and Nuessly 2008).

Control. Although no published information is available, experience with other cereal-feeding agromyzids suggests that the application of good sanitation methods (removal of crop residues, deep ploughing) in fields post- harvest is likely to reduce its incidence in subsequent seasons. A variation in susceptibility to attack has been shown in different maize cultivars in Egypt (Zeinab et al. 1991), although the target pest was likely misidentified. Goyal and Nuessly (2008) state that no chemicals are registered for the control of this leafminer in the USA. Spencer (1973) notes in a review of older literature that while this pest is expected to be problematic when it accumulates in large numbers, these numbers are generally kept in check by populations of local parasitoids. A review of North American species by Goyal and Nuessly (2008) includes eight species of hymenopterous parasitoids, seven eulophids and one braconid, but this does not include Opius utahensis Gahan (Hymenoptera: Braconidae), which was reared from the leafminer in Utah (Gahan 1913).

(Figs 27–34)

Identification & Diagnosis. The setae, abdomen and thorax (lightly pruinose) of Amauromyza flavifrons are dark brown, contrasting the head, which is yellowish-orange except for the brown first flagellomere, back of head, palpus, face and clypeus (Fig. 27). The legs are also brown with the apex of the fore femur yellow. There are often 5–6 fronto-orbitals, but sometimes as few as 3 on one side, the postvertical and ocellar setae are strong, nearly equal in length to the fronto-orbitals, there are 4 dorsocentrals, no prescutellar setae and the acrostichal setulae are in four scattered rows. The surstylus is fused to the epandrium and without spines (Figs 28, 29), and the distiphallus is black, bifid and twisted with minute spinules apically on the surrounding membrane (Figs 33, 34). Like other Amauromyza, the hypandrium is stout and broadly rounded (Fig. 30) and the ejaculatory apodeme has a broad, sclerotized “bowl”, although this bowl is pointed in A. flavifrons (Fig. 32). Wing length is 1.8–2.4 mm and the costa extends to vein M₁. The posterior larval spiracle has 3 bulbs, one of which is elongate (Spencer 1973).

Distribution. Amauromyza flavifrons occurs in the western Palaearctic Region (Spencer 1973; Martinez 2013), but it has been introduced into North America as early as 1964 in Ontario (Boucher 2012) and has spread throughout eastern North America to the west coast from Oregon to British Columbia, likely via accidental human-mediated transport on ornamentals.

•Nearctic Region: Canada (British Columbia, Ontario, Quebec), USA (widespread from New York to Minnesota and North Carolina; Oregon; Washington).

•Palaearctic Region: Albania, Belgium, Czech Republic, Denmark, Finland, France, Germany, Hungary, Italy, Kyrgyzstan, Lithuania, Netherlands, Norway, Poland, Romania, Russia, Spain, Sweden, Turkey, United Kingdom.

Hosts. Amauromyza flavifrons is a leafminer that is primarily recorded from plants in the family Caryophyllaceae (the “pinks”). Hosts include plants in the genera Agrostemma L., Cerastium L., Dianthus L., Gypsophila L., Moehringia L., Saponaria L., Silene L. [also records under the synonyms Lychnis L. and Melandrium Röhl.], Stellaria L. and Vaccaria Wolf (Benavent-Corai et al. 2005; Dempewolf 2004). Less frequent hosts include Beta vulgaris and Spinacia oleracea (Amaranthaceae). Laboratory experiments have shown that larval survival on B. vulgaris (beets) is lower than on caryophyll hosts (Scheffer 1999a). Genetic variation in larval survival on beets is lower than that of female oviposition choice, suggesting that populations of A. flavifrons in beet-growing regions may evolve to avoid oviposition on beets (Scheffer 1999b). Additional plants from which A. flavifrons has been reported include Lepidium L. (Brassicaceae), Bidens L. and Catananche L. (Asteraceae) (Gil-Ortiz et al. 2009; Lonsdale, unpublished data).

Damage. The larva forms a leaf mine in the upper or lower layer that is initially linear, but then becomes a conspicuous blotch that may obscure the initial linear mine. Individual larvae may move between and feed on both upper and lower mesophyll of the leaf. Multiple mines on single leaves may remove essentially all of the mesophyll. As with most agromyzid leafminers of adult leaves, low levels of abundance appear to have little effect on host plants, but larval feeding associated with large populations can result in significant damage. In the case of the occasional host Beta vulgaris, larval survivorship on the plant has been shown to be low (Scheffer 1999b), and damage to this crop is negligible. Potential economic impacts of leafmining to Dianthus and other ornamentals may be more pronounced (Spencer 1973) Because the leaves of these hosts, as well as spinach, are integral to crop value and a relatively small number of leaf mines on these can reduce market value.

Biology. Adult A. flavifrons mate within 24 hours of emergence in association with a host plant. Females oviposit through either the upper or lower leaf surface, and this can vary depending on host species. Eggs can be seen directly using a dissecting microscope, making this species amenable to studies of oviposition preferences and behaviours (Scheffer 1999a, 1999b). Larvae exit the leaves in order to pupate in the soil. Generation time in the laboratory is approximately one month, and in the U.S.A., there are multiple generations a year.

Movement & Dispersal. Movement appears to consist of association with the relocation of host plants, which include many commercial and garden ornamentals. Within North America, regional dispersal from household gardens is also likely as several ornamental hosts have naturalized extensively, including Saponaria officinalis L., Silene latifolia Poir. ssp. alba (Mill.) Greuter & Burdet, and Dianthus. In the U.S., these naturalized populations commonly support large populations of A. flavifrons.

Management. Early detection. A fact sheet on this species is available (Agromyzids of the World 2021).

Control. No specific information is available. Amauromyza flavifrons is attacked by a number of parasitoid wasps in the families Braconidae, Eulophidae and Pteromalidae (Spencer 1973). Conservation of parasitoids is likely to be an important means of regulating A. flavifrons populations (Spencer 1973).

“Cabbage Leafminer”

(Figs 35–42)

Other Common Names. Serpentine leafminer.

Identification & Diagnosis. Liriomyza brassicae is similar to most other Liriomyza in having a black notum with the shoulders (postpronotum+notopleuron) and a medial stripe on the scutellum yellow (Fig. 35). Wing length is 1.2–1.8 mm. The phallus is most diagnostic and should be examined for confident morphological identification, with the distiphallus being dark and barrel-shaped (Figs 40, 41)). The lateral margin of the frons along the eye is sometimes very narrowly brown (as in the imaged specimen in Fig. 35), differentiating it from similar pest species. The shape of the phallus sometimes varies slightly, as does external morphology and behaviour, which may be indicative of the presence of cryptic species (Lonsdale 2011; Tavormina 1982).

Distribution. Liriomyza brassicae has a nearly cosmopolitan distribution as a result of accidental human-facilitated transport. It is widespread in all biogeographic regions, but known distribution is patchy and it likely occurs in many more countries than those listed below (Deeming 2006; Etienne and Martinez 2003; Lonsdale 2011; Malipatil and Ridland 2008; Martinez 2013; Michalska 2003; Sasakawa 1977; Spencer 1977, 1989). It is likely widespread throughout much of the United States (Spencer 1973) and is frequently encountered in southern Quebec and Ontario, making it likely to occur across much of southern Canada. Within China, this species is known from Taiwan (Shiao et al. 1991) and from a female collected in Yunnan (Sasakawa 1986) to be considered suspect, but it is likely present throughout the country.

•Afrotropical Region: Cape Verde Is., Ethiopia, Kenya, Mozambique, Oman, Senegal, Spain (Canary Islands), South Africa, Yemen, Zimbabwe.

•Australian Region: Australia (widespread), Bonin Is., Fiji, French Polynesia (Austral Is, Gambier Is), Guam, New Caledonia, New Zealand, Northern Mariana Islands, Papua New Guinea, Solomon Islands, USA (Hawaii), Vanuatu.

•Nearctic Region: Canada (Alberta, Manitoba, Ontario, Quebec, Saskatchewan), USA (California, Colorado, Florida, Iowa, Maryland, Minnesota, Missouri, Montana, New York, Virginia, West Virginia, Wisconsin).

•Neotropical Region: Argentina, Brazil, Guadeloupe, Guyana, Martinique, Trinidad and Tobago, Saint Kitts and Nevis, Venezuela.

•Oriental Region: Cambodia, China (Taiwan, Yunnan?), India (Bihar, Delhi, Maharashtra, Punjab, Rajasthan, Uttar Pradesh), Indonesia, Japan (Ryukus), Malaysia, Philippines, Singapore, Sri Lanka, Thailand.

•Palaearctic Region: Egypt, France, Germany, Malta, Poland, Spain, Iraq, Japan, Romania, Saudi Arabia, Turkey.

Hosts. Liriomyza brassicae is a leafminer that is occurs frequently on Brassicaceae, especially on cabbage, cauliflower and broccoli (Brassica oleracea), but sometimes also Fabaceae (Lathyrus L., Pisum L.) and Tropaeolaceae (Tropaeolum) (Gil-Ortiz et al. 2009; Ipe and Sadaruddin 1984; Lonsdale 2011; Spencer 1973). Specimens have also been reared from Apiaceae (Foeniculum Mill.), Asteraceae (Ambrosia L., Dahlia Cav.), Capparaceae (Capparis L., Cleome L. [also as Gynandropsis DC]), Caryophyllaceae (Silene), Ranunculaceae (Aquilegia L.), Resedaceae (Reseda L.), Verbenaceae (Lantana L.) and Zygophyllaceae (Bulnesia Gay). Mines of L. brassicae have been recorded on Erysimum L., Lobularia Desv. (Brassicaceae) and Nicotiana L. species (Solanaceae) (see Spencer (1976)), but these records require verification.

The genera of Brassicaceae known to be attacked by this species are: Arabis L., Barbarea W.T. Aiton, Brassica L., Cakile Mill., Cardamine L., Diplotaxis DC, Erysimum L., Hirschfeldia Moench, Isatis L., Lepidium, Matthiola W.T. Aiton, Moricandia DC, Nasturtium W.T. Aiton, Raphanus L., Rorippa Scop., Sinapis L. and Sisymbrium L. (Frick 1959; Lonsdale 2011).

Damage. Damage to hosts is usually negligible unless the larvae occur in large numbers; in the latter case when there are multiple larvae per leaf, they may sometimes feed across the entire leaf surface, severely damaging photosynthetic potential. Feeding can destroy younger plants, but mature plants usually fare better, with larvae affecting mostly the outer foliage that will dry and drop off while the plant apex continues to develop (Spencer 1973). Some brassicaeous host species appear to perform better against larvae, with some being “resistant” or “tolerant” (Abdel and Ismail 1999). Degree of damage varies within and across localities and crops, but L. brassicae has the potential to grow to pestiferous levels with severe impact. Populations are regularly pestiferous in some areas, such as India, where the species is the most significant pest of Brassica rapa L. (as “Brassica campestris”; Singh et al. 1991).

Biology. Adult female flies seem to prefer young, medium sized shaded leaves for oviposition (Ipe and Sadaruddin 1984). Females may show a tendency to oviposit in the host that the population developed on (Tavormina 1982). On Tropaeolum majus L. (garden nasturtium), eggs are laid on the lower surface of leaves, generally at the margins (Beri 1974).

Larvae typically form a narrow, mostly linear to irregular or serpentine mine on the lower or upper leaf surface (feeding in the palisade and spongy mesophyll); mature larvae exit the mine for pupation in the soil (Beri 1974; Dempewolf 2004; Spencer 1973). Average development times of the immature stages on T. majus at about 28°C are: egg, 7.3 days; larva, 6.6 days; pupa, 9.2 days. Emergence generally takes place in the later hours of the day (Beri 1974).

Movement & Dispersal. Spencer (1973) reported that L. brassicae was the “most truly cosmopolitan species known in the Agromyzidae”. It is likely that the distribution of L. brassicae was influenced by trade, as with other major Liriomyza species of economic importance. However, that the broad distribution of this species was observed well prior to that of even the most polyphagous invasive Liriomyza species, suggests that movement via trade cannot fully explain the broad distribution.

Management. Early detection. For field monitoring, some of the information given for L. sativae and other polyphagous leafminers (in this volume) may be of relevance for L. brassicae.

Control. General information on control is available on the Plantwise database (Plantwise 2015). Plant hosts of low leaf phenolic content are more susceptible to attack but leaves with rough texture may repel oviposition even in plants with low phenolic content (Ipe and Sadaruddin 1984). Abdel and Ismail (1999) found that levels of glucosinolates within various Brassica species influence successful leafminer mines. Applications of glucosinolates onto infested cabbage substantially reduced the number of living miners. Singh et al. (1991) report that in India, flooding decreases the incidence of the leafminer in Brassica rapa fields and thus may be used as an alternative to insecticides. Early work reported that systemic organophosphates (e.g. phorate) were effective for the control of L. brassicae on cotton (Gossypium species) in Texas, USA (Davis et al. 1966) but this pest may represent a misidentification of either L. trifolii or L. sativae. More recent work in India on cabbage and other crops suggests that phenthoate (organophosphate), carbaryl (carbamate) and entomopathogenic nematodes can individually give good control compared with no treatments (Nimbalkar and Borle 1970). However, in Hawaii, USA, the leafminer is resistant to most insecticides apart from the translaminar cyromazine (an insect growth regulator) and abamectin (a neurotoxin) (Crop Knowledge Master 2016). As with other major economically important Liriomyza species, L. brassicae is attacked by a diversity of local chalcidoid parasitoids. These parasitoid communities exert a good level of natural control: e.g. in early work in California, USA on cabbage (Brassicae oleracea), average larval parasitism was 67.5% (Oatman and Platner 1969); and in Victoria, Australia, parasitism on Chinese cabbage (Brassica rapa var. pekinensis (Lour.)) reached 100% within six weeks of mines appearing (Bjorksten et al. 2005).

“Tomato Leafminer”

(Figs 43–48)

Identification & Diagnosis. Similar to most other Liriomyza, L. bryoniae has a black notum with the shoulders (postpronotum+notopleuron) and a central stripe on the scutellum yellow (Figs 43, 44). Wing length is 1.8–2.1 mm. The species belongs to a lineage of other polyphagous pests including L. huidobrensis, L. langei and L. strigata, diagnosed by a long membranous space between the pigmented section of the ejaculatory duct and the mesophallus, and a small distiphallus that is entirely divided medially, consisting of two short, pigmented tubules. The distiphallus of L. bryoniae, however, differs in having the apical tubules more broadly cup-shaped with a short, narrow base (Figs 47, 48) that in some illustrations appears very narrow and more abruptly constricted (e.g. Spencer 1973: figs 304, 305). Externally, this species is much paler than its relatives - the vertical setae are surrounded by yellow, the antenna is entirely yellow (Fig. 45; not including the arista; slightly pigmented in some Egyptian specimens (Spencer 1973)), the anepisternum is yellow with a small anteroventral spot, the brown spot on the katepisternum does not reach the base of the katepisternal seta (Fig. 43; an important character differentiating it from the related L. strigata, which has a brown marking behind the eye dorsum extend, or nearly extend to the base of the outer vertical seta (see Figs 50, 51)), and the femora are mostly yellow with sparse brown dorsal streaking.

The larval spiracles are shallowly semicircular with 7–12 pores (Spencer 1973: fig. 307). While adult males are relatively simple to diagnose morphologically, females and larvae are much more difficult, and published sequence data is recommended for comparison - e.g. Kox et al. (2005), Masetti et al. (2006) and Yang et al. (2013).

Distribution. Liriomyza bryoniae is a widespread pest in the Palaearctic Region from Europe to Japan, likely being present in most or all countries where favourable conditions permit development, and extends south into Oriental China, India and Vietnam (EPPO 2014). Wild populations are common in southern Europe and encountered with frequency in glasshouses further north (CABI & EPPO 2015a). Nearctic records have been proven invalid (EPPO 2014).

•Oriental Region: China (Fujian, Guangdong, Guangxi, Taiwan, Yunnan, Zhejiang), India (Maharashtra), Vietnam.

•Palaearctic Region: Albania, Austria (de Jong et al. 2020), Belarus (de Jong et al. 2020), Belgium, Bosnia and Herzegovina, Bulgaria, China (Anhui, Guizhou, Hainan, Hebei, Henan, Hubei, Hunan, Jiangsu, Jiangxi, Sichuan), Croatia, Czech Republic, Denmark, Egypt, Estonia, Finland, France, Germany, Greece, Hungary, Iran (Hazini et al. 2013), Iraq (Saleh et al. 2013), Ireland, Israel, Italy, Japan, Latvia, Lithuania, Malta, Moldova, Montenegro (Radonjić and Hrnčić 2011), Morocco, Nepal, Netherlands, Norway, Poland, Portugal, Republic of Korea, Romania, Russia, Slovenia, Spain, Sweden, Turkey, Turkmenistan, Ukraine, United Kingdom, Yugoslavia (de Jong et al. 2020).

Hosts. Liriomyza bryoniae is a leafminer that feeds on 112 host genera in 29 plant families (Benavent-Corai et al. 2005) including: Alismataceae, Amaranthaceae, Apiaceae, Araliaceae, Asteraceae, Basellaceae, Brassicaceae, Capparaceae, Caryophyllaceae, Chenopodiaceae, Crassulaceae, Cucurbitaceae, Dipsacaceae, Euphorbiaceae, Fabaceae, Gentianaceae, Hydrophyllaceae, Lamiaceae, Loasaceae, Malvaceae, Oxalidaceae, Pedaliaceae, Piperaceae, Polemoniaceae, Primulaceae, Scrophulariaceae, Solanaceae, Tropaeolaceae, Verbenaceae. Most host genera are Asteraceae, Brassicaceae, Cucurbitaceae, Fabaceae and Solanaceae. Populations are frequently pestiferous on curcurbits and tomatoes, but also on cabbage, lettuce and legumes.

Damage. In Europe and the Mediterranean Region, the species is considered a major pest of Asteraceae, Brassicaceae, Cucurbitaceae and Solanaceae, including colder regions where crops are grown in glasshouses (EFSA Panel on Plant Health et al. 2020a). Larval feeding results in lower yield via reduction of photosynthetic potential, leaf dwarfing, yellowing, drying, drooping and disfiguring, and sometimes fruit dropping and plant death; female oviposition and feeding punctures contribute to damage (Spencer 1973; Dempewolf 2004; CABI & EPPO 2015a). EFSA Panel on Plant Health et al. (2020a) noted that “in tomato, it was seen that yield losses can occur as a result of leafminer infestation but are not dependent on severity of damage alone; proximity to fruit at an early stage of development is very important”. Single larvae have been found to move through the stem via the petiole to multiple leaves if the young leaf / cotyledon is too small to support larval development, and multiple larvae are known to infest single larger mature leaves. Effects on younger plants, especially seedlings, are pronounced (Abul-Nasr and Assem 1961), and control measures in Cucumis melo whereby damage was delayed until later in plant development was successful in maintaining crop yield (Cheng 1994b). Liriomyza bryoniae is known to transmit the tobacco mosaic virus (Kalutskii 1992).

Biology. Eggs are laid mostly in the upper surface of cotyledons or young leaves, where larval mines predominate, but sometimes on the lower surface (FSA Panel on Plant Health et al. 2020). Mines are irregular to loose serpentine and not associated with the veins or midrib [see Dempewolf 2004; Spencer 1973 (figs 308–31)]. These mines are difficult to differentiate from those of other polyphagous species such as L. sativae and L. huidobrensis, although those of the latter more frequently occur along the midrib and lateral veins (Cannon et al. 2012; Spencer 1973). Spencer (1973) reports that larvae usually leave the mines and pupate in the soil, but studies by Saito (1988) on melon found that a higher percentage pupated on the leaves at higher temperatures.

Based on laboratory studies on tomato in the Netherlands, Minkenberg and Helderman (1990) found that the optimum temperature for reproduction and development within the range studied of 15–25°C, was at the upper value The lower threshold for development was 8°C and that for oviposition, 11°C. The net reproductive rate (R₀) varied from 9 (female eggs per female) at 15°C to 54 at 25°C; and the generation time from 49 to 22 days at the same two temperatures. In Japan, Cheng (1994a) found from studies on musk melons that the respective temperature thresholds for development of egg, larval pupal and total development were 7.05, 7.08, 7.7 and 7.38°C; and that the development times for these stages were 4.7, 93.2, 187.8 and 322.2 day-degrees. No significant development occurred at temperatures above 30°C. The life span of females 3–12 days and the mean eggs laid per female, 171.2.

Linden (1993) found that while the mortality of Liriomyza bryoniae pupae during winter months in the Netherlands was high, some can survive a season with 30 frost days and a lowest minimum temperature of minus 11.5°C.

Movement & Dispersal. Cheng (1994a) reports that in Taiwan, adults can travel long distances, facilitated by prevailing winds. On muskmelon plants, adults are most active within the plant canopy. In Japan, flight is diurnal with peaks at 06.00–08.00 and 14.00–16.00 hours.

Management. Early detection. Methods for early detection and subsequent monitoring in Western Europe are reviewed by Bell et al. (2013); yellow stick traps are considered the most efficient means for detecting adults.

Control. Successful trials with trapping in commercial greenhouses in Lithuania using yellow traps with the addition of synthetic methyl salicylate (a known plant-produced volatile compound) have been reported by Būda & Radžiutė (2008). Likewise, in Lithuania, successful trials with the photosensitizer hematoporphyrin dimethyl ether (HPde) used as photopesticides have been undertaken; HPde applied in a feeding bait and then irradiated caused the rapid death of adults, with females dying quicker than males (Lukšienė et al. 2007). Traditional broad spectrum insecticides [e.g. organophosphates (chlorpyrifos); carbamates (oxamyl); pyrethroids (permethrin)] or products developed later from the 1970s (e.g. the growth regulator cyromazine and the neurotoxin, spinosad) have been researched and/or are in use in several countries in the Old World; in general, pyrethroids and carbamates have been effective against adult flies, and cyromazine, spinosad and organophosphates are effective against larvae (Natskova and Karadzhova 1990; Tokumaru et al. 2005).

Reitz et al. (2013) summarized the history of resistance development of Liriomyza spp. against traditional broad-spectrum insecticides. In the European Union, the horticulture sector had to take steps to reduce insecticide use and develop integrated pest management (IPM) based on biological controls. This was because of the problem of insecticide resistance to broad spectrum products, and because of EU directives enacted in the 1990s relating to the phasing out of insecticides due to high human and environmental risk.

A diversity of hymenopterous parasitoids have been reported from the open field and/or glasshouses in several countries and/or regions; e.g. Western Europe (Nedstam 1983; Spencer 1973); Egypt (Neama et al. 2014); China – Taiwan (Lee 1990); Japan (Saito et al.1997). The species reported are mostly from the family Eulophidae (e.g. Diglyphus Walker spp.) although a few species are from the Braconidae (e.g. Dacnusa Haliday spp.). Much research has been done to underpin the conservation of species or their commercial use to protect glasshouse crops and this includes mass-rearing techniques; this work is reviewed by Liu et al.(2009). Good control has been achieved with Diglyphus isaea (Walker) in the Netherlands (Boot et al. 1992) and with a number of species in Russia (Ushchekov et al. 2002). Diglyphus isaea and Dacnusa sibirica Telenga are available commercially from biocontrol producers in Western Europe. The potential of entomopathogenic nematodes have been investigated in the UK (Williams and Macdonald 1995) and of bacteria in Kuwait (Al-Amad et al. 2001).

“Stone Leek Leafminer”

(Figs 55–61)

Identification & Diagnosis. Like most Liriomyza, L. chinensis is black with yellow shoulders (postpronotum + notopleuron) (Figs 55, 56), but the scutum has a greyish pruinosity, the scutellum is entirely black (medially yellow in almost all other Liriomyza), the calypter margin and hairs are white, the first flagellomere is pointed anterodorsally and the parafacial and orbital plate are raised (Fig. 57). Wing length is 1.5–1.9 mm. The phallus (Figs 58, 59) is highly diagnostic and much larger than that of similar taxa, with one pair of long dark tubules mostly surrounded by a similarly dark, broad basal sheath with a short, narrow stem (=mesophallus). The surstylus is missing a spine, but this may be represented by the additional spine on the inner-ventral surface of the epandrium (Fig. 60). The larvae have 7–8 pores on the anterior spiracle and 8–10 on the posterior spiracle, similar to L. cepae (Hering).

Other Allium feeders include the continental European L. cepae and L. nietzkei Spencer, which are also dark in colouration with a white calypter and an angulate first flagellomere. The former also has an entirely black scutellum, but the margin of the head behind the eye is paler, the coxae and dorsum of the femora are brown, the sheath surrounding the tubules of the distiphallus is a short basal bowl, and the body is larger with a wing length of 2.0–2.5 mm. The latter has a scutellum narrowly to broadly yellow medially, the distiphallus is much smaller with a shallow basal bowl and the mesophallus is considerably longer. While sequence data for these two European species are not available, mitochondrial and nuclear gene sequences exist for L. chinensis, which can aid in differentiation from other major crop pests (Chiu et al. 2000; Kox et al. 2005; Scheffer et al. 2006), although external morphological data should be sufficient in these instances. Tokumaru et al. (2021) found two mitochondrial biotypes of L. chinensis that may be associated with two different mine types of L. chinensis on Welsh onion in Japan.

Distribution. Liriomyza chinensis is known from the eastern Palaearctic Region and parts of the Oriental Region into southeast Asia, but also recently from France, Germany and Russia (Artokhin 2009; Chen et al. 2003; Dempewolf 2004; Scheffer et al. 2006; Malipatil and Ridland 2008; Pan and Jiang 2001; Santosh and Bhuiya 2014). Within China, there are few records in both the Palaearctic and Oriental Regions of that country, but the species is likely much more widespread. Mines from the Kirghiz Republic have been attributed to this species (Dovnar-Zapolski 1969), but could also belong to either L. cepae or L. nietzkei (Spencer 1973).

•Oriental Region: Bangladesh, China (Taiwan, Zhejiang), Indonesia, Malaysia, Philippines, Singapore, Thailand, Vietnam.

•Palaearctic Region: China (Beijing, Inner Mongolia, Shandong), France, Germany, Japan, Kirghiz Republic(?), Republic of Korea, Russia.

Hosts. Liriomyza chinensis is a leafmining pest of Allium spp. (Alliaceae), known from A. ampeloprasum L., A. cepa L., A. chinense G. Don, A. fistulosum L., A. odorum L. (Martinez 1982) and possibly A. sativum L. (Dempewolf 2004).

Damage. Larvae of this species lessen the health of plants by mining in and destroying leaves, and in some instances can be a primary crop pest (Ahn et al. 1991). While they can be considered severe pests, outbreaks are infrequent with only local occurrences (Dempewolf 2004).

Biology. General life cycle is similar to other polyphagous Liriomyza species (this volume). In laboratory studies in Japan at 25°C and 16L:8D photoperiod, L. chinensis females had an average life span of 9 days and laid an average of 108 eggs, and feeding and fecundity peaked at 5 days (Tran and Takagi 2005a); in the same study, development time from egg to adult in the laboratory was 22.6 days and it was found that the time for pupal development lasted slightly longer than the combined egg and larval stages. In further studies on the development time of immature stages (Tran et al. 2007a) it was found that development was inversely proportional to temperature from 15–30°C, ranging from 69.6 days at the former temperature to 17.1 days at the latter; development time began to increase at 32.5°C. The development time from egg to adult was 312.5 day-degrees above a threshold of 11.4°C. Tan and Takagi (2007) showed that cold hardiness of pupae rapidly decreases at low temperatures and extended exposure times: survival is zero below 5°C with 16 days of chilling but rises to 42.9% at 10°C. Using this information, these authors estimated that the species would be able to overwinter in the field in southern Japan, but not in the northern part of the country. The mines may appear continuous, but are sometimes also discontinuous, with the larva alternating between feeding below the epidermis and the inner cell layer along the hollow stem surface (Tokumaru et al. 2021, see Identification, above).

At 22.5°C the net reproductive rate (R_o) was 14.3 days and the generation time (GT) 27.1 days (Tran and Takagi 2005a).

Movement & Dispersal. The possibility for long-distance dispersal is significant if anecdotal evidence is correct in that puparia lodge in the skins of onion and are thus able to be transported internationally (Malipatil and Ridland 2008).

Management. Early detection. No published information is available but some of the information on field monitoring given for L. sativae and other polyphagous leafminers may be of relevance for L. chinensis.

Control. No published official guidance for control of the pest is available, but Tran and Takagi (2005b) and Tran et al. (2006) assessed conventional insecticide use by farmers for control of L. chinensis in Vietnam and Japan. Using field trails and the recommended field rates, cartap (a thiocarbamate), permethrin (a pyrethroid) and phenthoate (an organothiophosphate) were found to have little or no impact on larvae or adults. However, the translaminar insecticide cyromazine (an insect growth regulator) was effective for the control of larvae. Tran and Takagi (2006) reported that the endoparasitoid Neochrysocharis okazakii Kamijo (Eulophidae: Hymenoptera) is a dominant natural enemy of the leafminer in Vietnam and provided a report on its biology. In a study of hosts suitable for mass-rearing of this parasitoid for augmentative releases, Tran et al. (2007b) showed that L. trifolii is more suitable than L. chinensis because the intrinsic rate of increase (r_m) of the parasitoid is higher on the former.

“European Pea Leafminer”

(Figs 62–68)

Identification & Diagnosis. Liriomyza congesta is similar to other Liriomyza externally in having a black notum with the shoulders (postpronotum+notopleuron) and a wide medial stripe on the scutellum yellow (Figs 62, 63). Wing length is 1.3–1.7 mm. Similar to many other species, including other Fabaceae-feeders, it has a lightly grey pruinose scutum, two rows of acrostichal setulae (not four), and pale colouration including a wide yellow space on the head around the base of the vertical setae (not brown) (Fig. 64), a yellow anepisternum with a small brown anteroventral spot, a small brown spot on the katepisternum that does not reach the base of the katepisternal seta and yellow femora that are narrowly brown basally. Due to this external similarity to congeners, examination of the male genitalia is required for confident diagnosis: the phallus includes a dark stem-like mesophallus and a broad, bowl-shaped distiphallus enclosing one pair of short, wide tubules (Figs 65, 66). Typical of a species in the L. hieracii group, a dark bar with a terminal spine can be seen inside the ventral surface of the epandrium (Fig. 67). The posterior larval spiracle has 3 pores.

A similar phallus is seen in the Nearctic Liriomyza fricki Spencer (Lonsdale 2011: Figs 106, 107), which also feeds on a variety of Fabaceae, but the distiphallus of this species is much larger, bulging dorsally across the surface of the mesophallus, and the inner surface of the “bowl” is minutely textured (not smooth).

Liriomyza pisivora Hering also occurs on Lathyrus and Pisum in Europe, but the anterior two dorsocentrals are setula-like, the posterior larval spiracle has 7–8 pores (Spencer 1973) and the phallus is highly derived (see Dempewolf (2004) and Spencer (1973: figs 132–133)).

Distribution. Liriomyza congesta is widespread across the Palaearctic Region, especially in Europe and North Africa, with most cases of crop damage occurring in Mediterranean countries; it has also been found in the southern Arabian Peninsula and India (Kashmir) (Dempewolf 2004; Deeming 2006; Černý 2013; Martinez 2013). Early records of this species in the New World are misidentifications of L. trifolii (Burgess) (Spencer 1973).

•Afrotropical Region: Oman, Yemen.

•Oriental Region: India (Kashmir).

•Palaearctic Region: Afghanistan (Spencer 1976), Albania, Andorra, Austria, Belgium, China (Ningxia) (Liu et al. 2005), Croatia, Czech Republic, Cyprus, Denmark, Egypt, Estonia, Finland, France, Germany, Greece, Hungary, Iran (Dousti 2010), Iraq (Saleh et al. 2013), Ireland, Israel, Italy, Japan, Republic of Korea, Latvia, Lithuania, Malta, Moldova, Netherlands, Norway, Poland, Portugal (mainland, Madeira), Romania, Russia, Slovakia, Spain (mainland, Canary Islands), Sweden, Switzerland, Turkey, United Kingdom and the former Yugoslavia.

Hosts. Liriomyza congesta is a leafminer that feeds on 27 genera of Fabaceae (Benavent-Corai et al. 2005), including: Anthyllis L., Astragalus L., Caragana Fabr., Cicer L., Colutea L., Coronilla L., Glycine, Glycirrhiza L., Hippocrepis L., Hymenocarpos Savi, Lathyrus, Lens Mill., Lotus L., Lupinus, Medicago, Melilotus, Onobrychis Mill., Ononis L., Ornithopus L., Oxytropis DC, Phaseolus, Pisum, Robinia L., Scorpiurus L., Trifolium, Trigonella L., Vicia L. Lathyrus, Pisum and Vicia are considered primary hosts (Spencer 1973, 1990). Specimens have also been reared from Spanish Euphorbia L. (Euphorbiaceae) (Docavo et al. 1987).

Damage. Populations uncommonly occur in numbers sufficient enough to cause more than minor damage (Spencer 1973), although outbreaks sometimes occur where the mines can cover most of the leaf surface and severely impede photosynthetic potential, weakening the plant and reducing fruit production. In Egypt, it has been considered one of the most important pests of Vicia faba L. (El-Khouly et al. 1997b).

Biology. Dimetry (1971) published aspects of the life cycle and biology of this species on Vicia faba in Egypt. It was misidentified as L. trifolii even though Spencer (1965) had clarified that the pest species on this host in Egypt was L. congesta.

Mating takes place shortly after adult emergence: 8 hours in summer (May – June) and 1.6 days in winter (February). Eggs are typically located on the lower surface of primary and secondary leaves. The larvae create a linear to irregular mine on the upper surface of the leaf, usually with one larva per leaf. In the laboratory, duration of female oviposition period as well as fecundity are influenced by nutrition quality and temperature. Oviposition period primarily depends on temperature, ranging from 5–11 days in the summer and 7–23 days in the winter. Fecundity is greatly influenced by nutrition. Under laboratory conditions, maximum egg production was at 20°C and unfed females provided with only distilled water produced no eggs. Females fed with honey produced a mean of 135 eggs, those fed with sugar and yeast produced a mean of 79 eggs, and those fed with sugar solution produced a mean of 55 eggs. Overall, adults provided with a mixture of sugar and yeast lived longer (approximately 24 days females and 19 days males) than those without food.

Dimetry (1971) found that development times of immature stages in the laboratory were inversely proportional to increasing temperature from 20–35° C. At 20°C, the egg stage lasted a mean of 4.9 days, the larval stage a mean of 10.4 days and the pupal stage a mean of 12.7 days. Pupation takes place outside the leaf and usually in the soil below the plant. Temperature and humidity both influence survival of the pupae with the optimum conditions for adult emergence being 20°C and 100% RH. El-Khouly et al. (1997a) also reported that ambient temperature and RH account for changes in the population density of larvae on broad bean in the field.

Movement & Dispersal. No available published data, but horticultural trade involving peas may pose a risk of human aided dispersal.

Management. Early detection. For field monitoring, some of the information given for L. sativae and other polyphagous leafminers may be of relevance for L. congesta.

Control. Several authors (Bastawisy et al. 1998; El-Khayat 1998; El-Khouly et al. 1997b) report variability in resistance between Vicia faba cultivars in Egypt with some cultivars showing reasonable degrees of resistance. Grill (1979) states that yellow sticky traps have been used successfully in France to control adults in glasshouse ornamentals production. Abbasi, Ghassemi-Kahrizeh and Hosseinzadeh (2021) investigated the effects of planting date and cultivar on yield in Cicer arietinum L. in Iran and found singnificat effect of both as well as their interaction. Several organophosphates have been trialed on V. faba in Egypt but the work is quite old and recent updates are not available. Among the more effective were fenthion and phosalone (contact insecticides) and formothion and methamidophos (contact and systemic action insecticides) (Assem et al. 1975; El-Kifl et al. 1974; Rizkalla et al. 1970). More recent trials of generally more effective insecticides were made against against Liriomyza trifolii, including the neurotoxin abamectin (Saad et al. 2007) and may be effective for use against L. congesta. In Egypt, L. congesta on V. faba is attacked by several local chalcidoid (Hymenoptera) parasitoids (Hafez et al. 1974) including larval parasitoids (Diglphus sp.and Hemiptarsenus zilahisebessi Erdős) and pupal parasitoids (Opius Wesmael sp. and Halticoptera Spinola sp.). Diglphus sp. and Opius sp. were common throughout most of Egypt. Parasitism of the leafminer was recorded on beans plants not long after the first infestations of the leafminer were observed, reaching a rate of 75% towards the end of the growing season.

“Pea Leafminer”

(Figs 69–73)

Other Common Names. Serpentine leafminer; South American leafminer; potato leafminer; minador de la hoja, minador pequeño, mosca minadora (Spanish).

Identification & Diagnosis. Liriomyza huidobrensis is a relatively dark species of Liriomyza, the species of which are usually characterized by a black notum with yellow shoulders (postpronotum+notopleuron) and a yellow medial stripe on the scutellum (Figs 69, 70) (as for the related L. langei – Figs 74, 75). In this species, described and illustrated in Lonsdale (2011), wing length is 1.9–2.7 mm, black pigment covers most of the pleuron (at least the dorsal 1/3 of anepisternum is yellow), all of the abdominal tergites, and most, if not all of the femora exclusive of the apices. The acrostichal setulae are also usually in 2–3 rows (less commonly 4), and the posterolateral corner of the frons is dark to at least the base of the outer vertical seta.

The genitalia are characterized by a phallus with a long, clear section of the ejaculatory duct in between its subapical pigmented section and the mesophallus, and the distiphallus is entirely split into two short, dark tubules (Figs 72, 73). A similar phallus occurs in other pestiferous species, including the predominantly Nearctic L. langei Frick (Figs 79, 80), which was once considered conspecific but was resurrected from synonymy and recharacterized by Scheffer (2000), Scheffer and Lewis (2001) and Lonsdale (2011). Liriomyza langei always has 4 rows of acrostichal setae (Fig. 74), there is a slight gap between the pigmented section of the ejaculatory duct and the hypophallus (Lonsdale (2011: figs 129–131)), and the orbital plate is usually darker. Morphological diagnosis is problematic, however, especially considering the degree of overlap between the two species, and molecular techniques for differentiation is recommended whenever possible. Recommended methodologies were presented in Scheffer et al. (2001), Nakamura et al. (2013) and Scheffer et al. (2014). The Nearctic L. trifoliearum Spencer, also an occasional pest on Fabaceae and Solanum L., is similarly dark and with a similar phallus, but the paraphalli are larger, triangular, divergent and wing-like (Lonsdale 2011).

Similar related polyphagous pests in the Old World include Liriomyza bryoniae (Fig. 43) and L. strigata (Fig. 49), which are paler and have an apically widened distiphallus.

Larvae are small and typically maggot-like. The posterior spiracle forms a crescent with six to nine raised pores (Spencer 1973: fig. 319).

Distribution. Liriomyza huidobrensis is native to cooler highland areas in South America (Steck 1996), and maybe also Central America (Scheffer and Lewis 2001; Lonsdale 2011; but see Weintraub et al. (2017)). It is now widespread globally due to human-facilitated transport (Lonsdale 2011; EPPO 2014), at first likely via the flower trade, as discussed in Weintraub et al. (2017). Its recent appearance in Sydney (New South Wales Department of Primary Industries 2020) marks a new milestone in continental dispersal. It is competitive with other sympatric invasive leafminers in cooler climates or higher elevations (Tantowijoyo and Hoffmann 2010). Occurrences in North America are surprisingly few, although populations have been problematic in glasshouses in Canada, and there are several records from California (Lonsdale 2011). Subsequent surveying of Californian crops by Scheffer (et al. 2014), however, suggests that these Californian records are misidentifications, and that there is no evidence for the presence of the species in that state.

•Afrotropical Region: Comoros, Kenya, Mauritius, Rėunion, Seychelles, South Africa, Tanzania, Zambia, Zimbabwe.

•Australian Region: Australia (NSW (New South Wales Department of Primary Industries 2020)), Easter Island, Guam.

•Nearctic Region: Canada (possibly restricted to glasshouses in Alberta, British Columbia, Ontario, Nova Scotia).

•Neotropical Region: Argentina, Belize, Brazil (Goiás, Minas Gerais, São Paulo), Chile (widespread, inc. Juan Fernandez Isl.), Colombia, Costa Rica, Dominican Republic, Ecuador, El Salvador, French Guiana, Guadeloupe (not established), Guatemala, Honduras, Mexico (Mexico State?), Nicaragua, Panama, Peru, Uruguay, Venezuela.

•Oriental Region: Bangladesh, Cambodia (presence uncertain, intercepted on exports), China (Fujian, Guangdong, Yunnan), India (Uttar Pradesh), Indonesia (Java, Sulawesi, Sumatra), Malaysia, Philippines, Singapore, Sri Lanka, Taiwan, Thailand, Vietnam.

•Palaearctic Region: Arabian Peninsula, Austria, Belgium, Bulgaria, China (Gansu, Guizhou, Hebei, Hubei, Inner Mongolia, Shaanxi, Shandong, Sichuan, Xinjiang), Crete, Croatia, Cyprus, Czech Republic, Korea (Democratic People’s Republic of), Finland, France, Germany, Greece, Hungary, Israel, Italy, Japan, Jordan, Korea (Maharjan et al. 2014), Lebanon, Malta, Montenegro, Morocco, Syria, Poland, Portugal, Serbia, Spain, Sweden (intercepted only), Switzerland, Turkey. Eradicated from Denmark, Ireland, Lithuania, Norway, United Kingdom.

Hosts. Liriomyza huidobrensis is a broadly polyphagous leafminer that feeds on many food and ornamental crops. It attacks at least 365 plant species in 49 families (Weintraub et al. 2017): Adoxaceae, Aizoaceae, Alstroemeriaceae, Alismataceae, Amaranthaceae, Amaryllidaceae, Apiaceae, Apocynaceae, Araceae, Araliaceae, Asparagaceae, Asphodelaceae, Asteraceae, Balsaminaceae, Basellaceae, Brassicaceae, Campanulaceae, Caryophyllaceae, Convolvulaceae, Cucurbitaceae, Euphorbiaceae, Fabaceae, Gentianaceae, Gesneriaceae, Hydrangeaceae, Iridaceae, Lamiaceae, Liliaceae, Linaceae, Malvaceae, Menispermaceae, Moraceae, Onagroideae, Oxalidaceae, Papaveraceae, Plantaginaceae, Plumbaginaceae, Poaceae, Polemoniaceae, Polygonaceae, Portulacaceae, Primulaceae, Ranunculaceae, Rosaceae, Scrophulariaceae, Solanaceae, Tropaeolaceae, Verbenaceae, Violaceae. Studies have reported preferences for some species of host plants, especially within Solanaceae (eg. Okoth et al. (2014)) and Fabaceae (eg. Baoping et al. (2006), Videla et al. (2006); but see Martin et al. (2005)), but females can oviposit in a variety of available hosts to produce robust offspring, although performance measures will vary to some degree (Martin et al. 2005).

Due to historical difficulties in differentiating Liriomyza huidobrensis from L. langei, published host records from the Nearctic are sometimes confused for the two taxa, but this issue was largely resolved by Lonsdale (2011). Since L. langei is now known to have a restricted distribution (western USA, Hawaii, possibly Mexico), published records of these taxa from the Old World (excluding Hawaii) and eastern North America actually refer exclusively to L. huidobrensis.

Damage. Damage to several vegetable crops (e.g. beans, peas, potato, tomato) and ornamental plant species have been reported largely from the open field in subtropical and tropical regions and from protected horticulture in temperate climates (CABI 2015b). Field potatoes have been particularly badly affected and the leafminer remains an issue on this and other crops in many countries and regions including Peru (ICIPE 2015; Mujica and Kroschel 2011), Argentina, Brazil, Costa Rica, Guatemala (Weintraub et al. 2017), Kenya (Foba et al. 2015; ICIPE 2015) and Indonesia (Rauf et al. 2000; Shepard et al. 1998). Severe outbreaks of the pest in Israel in the early 1990s (Weintraub and Horowitz 1995) subsided after very high temperatures in 1998 and it is now considered an occasional pest (Weintraub 2001a). Likewise, field grown Pisum sativum cultivars (sugar and snow peas) for export markets in Kenya are affected and this threatens the livelihoods of small holders who rely on horticultural cash crops for income (Gitonga et al. 2010).

In temperate Europe, Liriomyza huidobrensis became a pest from the late 1980s and early 1990s on protected horticulture but also on outcrops in the Mediterranean region (CABI 2015b). Crops affected include: Chrysanthemum, Primula L., Verbena, lettuces, beans, Cucumis sativus L., Apium graveolens and squashes/pumpkins (CABI 2015b).

Mining activity in the leaves of infested plants causes a reduction in photosynthetic activity (Parrella 1987). This can lead to a delay in the development of young plants, yield loss and leaf damage in ornamental plants (CABI 2015b; Parrella 1987). On Solanum tuberosum (potato), larval infestations start in the lower part of the plant, but damage is not as severe in growing plants as fully mature plants (Mujica and Cisneros 1997). There is a correlation between the presence of Liriomyza huidobrensis and the pathogenic fungus Alternaria solani Sorauer on potato (Soares et al. 2019).

Biology. The biology of this species has been recently reviewed by Weintraub et al. (2017). The life cycle is similar to other multivoltine agromyzids. Considerable research on the effects of temperature on oviposition, longevity, and larval growth and survival (Olivera et al. 1993; Chen and Le 2004). Host plant leaves are punctured by adult females for feeding and eggs are laid just below the leaf surface (Mujica and Cisneros 1997). Both feeding and oviposition are favoured by cooler temperatures (Olivera et al. 1993). The larvae of L. huidobrensis mine the chloroplast-containing spongy mesophyll layers, disrupting photosynthesis more than other leafminers that mine the palisade mesophyll layer (Parrella 1987). The larval mines are usually close to the leaf midrib and lateral veins (CABI 2015b). In Peru, females lived 3–28 days and males 2–6 days. Females laid an average of 117 eggs in winter and 161 in the spring. The egg stage lasts 3–4 days, the first instar larval stage 3–4 days, the second instar larval stage 2–3 days, the third instar larval stage 3–4 days, and the pupal stage 12–18 days (Mujica and Cisneros 1997). On lettuce as a host, the estimated minimum developmental temperature thresholds for the three larval stages and pupal stage were 5.4, 6.3, 6.2 and 5.7°C respectively; and the day-degree days for these stages were 84.3, 30.1, 58.9 and 143.7 respectively (Head et al. 2002). Mujica et al. (2017) investigated survival of all four life stages, female fecundity, and adult longevity across seven temparatures ranging from 10–35°C, and concluded that L. huidobrensis development requires a temperature between 12–28°C.

There have been a large number of studies on female oviposition preferences for different host plant species as well as for varieties within host species (Wei et al. 2000; Martin et al. 2005; Baoping et al. 2006; Videlia et al. 2006; Liying et al. 2008; Videlia et al. 2012; Maharjan and Jung 2016; Weintraub et al. 2017). In a laboratory study on Pisum sativum, Solanum tuberosum, Lactuca sativa, gai lan (Brassica oleracea), Apium graveolens (celery) and Cucumis sativus (cucumber), adults preferred Cucumis and gai lan for oviposition; but no difference was found in the proportion of adult emergence from the six crops (Martin et al. 2005). In Israel, adult flies are present in the field from the autumn through to the spring but not in summer (Weintraub and Horowitz 1996).

Movement & Dispersal. Studies using yellow sticky traps in potato crops in Israel showed that peak activity of the adults occurs in May and June. Adults are most active just after sunrise, with activity gradually decreasing during the day; activity in the morning was inversely correlated with temperature. Adults are less active at ground level, preferring to be at 0.2 m or more above the top of plants (Wientraub and Horowitz 1996).

As with other highly polyphagous Liriomyza species, long-distance dispersal of Liriomyza huidobrensis is human-facilitated and driven by the development of the global horticultural trade (Parrella and Keil 1984; Weintraub et al. 2017). Research in China has shown that the cold tolerance of L. huidobrensis pupae increases with latitude up to 35°N and that cold tolerance of populations was enhanced by pre-chilling pupae at 0°C, 5°C and 10°C. Beyond this latitude, the leafminer can only survive in protected habitats such as glasshouses (Chen and Kang 2004). A temperature-based phenological model Mujica et al. (2017) has been developed to allow prediction of life-stage parameters and population growth of L. huidobrensis in various climates.

Management. Early detection. Liriomyza huidobrensis is now widely distributed in the Old and New Worlds and is considered a major quarantine pest by many countries. There are many fact sheets on the leafminer available, including CABI (2015b) and Steck (2011). A plant health risk assessment for south Florida, USA, based on the temporal and spatial analysis of temperature data for the south and the day-degree development of the leafminer showed that the likelihood of breeding populations establishing was high (Milla and Reitz 2005). A broader assessment of the risks to plant health for the European Union concluded that the risk of establishment and spread was high because the leafminer is already present in many countries of the region and the pest can easily be moved with plant material. Overall impact was rated as minor for Mediterranean countries but in non-Mediterranean countries, impact was rated as moderate under protected crops and minor on outdoor crops (EFSA Panel on Plant Health 2012).For risk management, OEPP/EPPO (1990) recommended that plant propagating material of a defined list of vegetable crop and ornamental flower species from countries where the pest occurs must be inspected at least every month for three months and found to be pest free before transport. A phytosanitary certificate should also be issued for cut flowers and vegetable crops with leaves. EFSA Panel on Plant Health (2012) recommend ways in which risk management procedures could be tightened. For field monitoring, yellow sticky traps were used with effect by Weintraub (2001a) for the field monitoring of adult fly populations in Israel. Dankowska et al. (2000) also used these traps in Polish glasshouses but they laced the traps with 3-phenylopropioaldehyde to improve catch rate. Sampling plans for L. huidobrensis have been developed in several crops and locations, generally with the goal of facilitating decision making for IPM management. Alves et al. (2014) and Lopez et al. (2019) provide specific plans for estimating mines on potato and tomato crops, respectively, in Brazil.

Control. Management of vegetable waste, a source of new leafminer populations, was found to be effective for ornamental flower production in Italy (Bosio 1994). In Costa Rica, optimum sticky trap colour was found to be yellow (Weintraub et al. 2017); Civelek et al. (2004) found that mass trapping with yellow sticky traps and the use of exclusion nets were effective for cucumber production in glasshouses in Turkey. Intercropping for pepper (Capsicum annuum L.) production using sugar cane (Saccharum officinarum L.) increased local parasitism rates in China (Chen et al. 2011) and Valencia and Campos (1980) reported on the identification of some potato varieties showing some degree of resistance to attack. A range of insecticides are currently applied by farmers in tropical regions in attempts to control L. huidobrenis. Many products in use include conventional insecticides such as carbamates, pyrethroids and organophosphates (e.g., ICIPE 2015; Rauf 2000), and it is known that invasive highly polyphagous Liriomyza species rapidly develop resistance to these (Reitz et al. 2013) and resistance in L. huidobrenis was reported from the first outbreaks of the pest in South America in the early 1970s (Weintraub and Horowitz 1995). These products are also highly toxic to parasitoids (Reitz et al. 2013). Effective control of pea leafminer larvae has been achieved in trials with the translaminar insecticides cyromazine (an insect growth regulator), abamectin and spinosad (neurotoxins) in Israel (Weintraub and Horowitz 1998; Weintraub 2001b; Weintraub and Mujica 2006), the first two insecticides in Indonesia (Hidrayani et al. 2005) and the first in European glass houses (CABI 2015b). Current research suggests that these insecticides are more compatible with insect parasitoid biological control agents than conventional insecticides, but abamectin and spinosad are toxic to adult wasps, and are more toxic than cyromazine (Reitz et al. 2013; Weintraub and Horowitz 1998). Abamectin is also toxic to the entomopathogenic nematode Steinernema feltiae Filipjev but the organophosphates trichlofon and dimethoate are not (Head et al. 2000). In a global review of the biology and management of L. huidobrenis Weintraub et al. (2017) report that 106 parasitoid species have been reared from the leafminer. In the native range of the leafminer Salvo et al. (2005) using trap plants showed that parasitoid species diversity on this leafminer is high in Argentina and that overall parasitism is not lower in cultivated versus natural habitats; parasitism levels sometimes exceeding 50% in the former. Parasitoid diversity has been found to be relatively high in some parts of the adventive range, including Europe (EFSA 2012) and Indonesia (Rauf et al. 2000). Furthermore, a predatory fly, Coenosia humilis Meigen (Muscidae) has been reported as being common and important in control in Indonesia (Hidrayani et al. 2005). In Kenya, an introduction of parasitoid species from Peru has been made to complement conservation measures of local parasitoids, and the species Phaedrotoma scabriventris Nixon (Hymenoptera: Braconidae) has been released in the vegetable growing areas of the Central Highlands (ICIPE 2015). Several types of biological control agent have been researched/are being used for use in European glasshouses. The parasitoids Dacnusa sibirica (Braconidae) and Diglyphus isaea (Eulophidae) are produced commercially and used in combination for glasshouse crops early in the season but only Diglyphus is used later in the season when temperatures rise (van der Linden 2004). Numerous studies in Europe have also demonstrated significant parasitism levels from native parasitoid species that move into glasshouses naturally (EFSA 2012). Research has shown the potential of using entomopathogenic nematodes, particularly Steinernema feltiae, in foliar applications on glasshouse crops against the leafminer larval stages (William and Waters 2000). Further work has shown that this nematode causes high mortality of parasitoid larvae (Head et al. 2003).

“California Pea Leafminer”

(Figs 74–80)

Othe Common Names. Liriomyza langei has been referred to in the past as the “pea leafminer”. This is no longer recommended as it may cause confusion with L. huidobrensis, a widespread global invasive species and former senior synonym.

Identification & Diagnosis. Liriomyza langei is a relatively dark species of Liriomyza, most species of which have a black notum with yellow shoulders (postpronotum+notopleuron) and a yellow medial stripe on the scutellum (Figs 74, 75). This species is highly similar to the globally distributed L. huidobrensis, with which it was once considered conspecific, but later resurrected by Scheffer and Lewis (2001). The diagnostic phallus of L. langei (Figs 79, 80) is very similar to that of L. huidobrensis (Figs 72, 73), composed of one pair of short, dark and entirely divided tubules. Liriomyza langei, however, has a restricted, non-overlapping distribution, there are always 4 rows of acrostichal setulae (often 2–3, but sometimes 4 in L. huidobrensis), wing length is slightly smaller (1.6–2.3 mm), the orbital plate is usually darker and there is no gap between the pigmented section of the ejaculatory duct and the hypophallus. Considering the difficulties involved in diagnosing these species, molecular techniques are recommended following initial morphological screening, as outlined in Scheffer et al. (2001), Nakamura et al. (2013) and Scheffer et al. (2014).

Distribution. Liriomyza langei is widespread in California, but also extends to Oregon, Washington, Texas and Mississippi, and has been introduced into Hawaii (Scheffer et al. 2001). Populations reported from Florida, Utah and Virginia did not establish (Steck 1996). It is suspected that Mexico, at least in regions adjoining California, also hosts populations of the species, reinforced by the presence of these flies in intercepted shipments originating in an unknown location within Mexico (Takano et al. 2005).

Hosts. Liriomyza langei is a leafminer recorded from seventeen families: Amaranthaceae, Apiaceae, Asteraceae, Brassicaceae, Caryophyllaceae, Chenopodiaceae, Convolvulaceae, Cucurbitaceae, Fabaceae, Gnetaceae, Liliaceae, Liliaceae, Primulaceae, Solanaceae, Turneraceae, Valerianaceae, Violaceae. An updated catalogue of host plant genera for Liriomyza langei was provided by Lonsdale (2011).

Damage. Liriomyza langei was reported causing economic damage to peas (Pisum sativum) but also to celery (Apium graveolens), spinach (Spinacea oleracea), sugar beet (Beta vulgaris) and asters in California in the late 1940s (Frick 1951). Since this time further outbreaks have been reported from California and other areas in the USA: in California, Elmore and Ranney (1954) reported damage to seedling chili pepper plants (Capsicum), causing considerable yield losses, but more mature plants were not affected; also in California, Lange et al. (1957) reported serious damage to autumn Spinacia oleracea; in Mississippi, Davis et al. (1969) reported damage to snap beans (Phaseolus vulgaris) and peas (Pisum sativum); in Texas, Chow and Heinz (2005) inferred that the leafminer was a problem on Chrysanthemum in semi-protected field production systems; and in Florida, Poe and Montz (1981) reported an outbreak (as ‘L. huidobrensis’) in a field of Gypsophila that was assumed to originate from transported nursery stock from an infested area in California.

Since these reports, in California at least, the leafminer varies in pest status from ‘a sporadic fall (= autumn) pest, relatively easily controlled, to a pest throughout most of the vegetable growing season that is essentially not able to be controlled in many crops’ (Steck and Dixon 2006). Lettuce is the most highly affected crop (Steck and Dixon 2006). Damage to crops is primarily caused by the mining of leaves by the larvae but Steck and Dixon (2006) report that feeding punctures can kill seedlings and reduce photosynthesis. Costa et al. (1958) and Bennett and Costa (1961) showed from studies in California that the leafminer can transmit (via plant sap) sowbane mosaic virus to sowbane (Chenopodium murale (L.) S. Fuentes, Uotila & Borsch) and tobacco mosaic virus from various sources to sowbane and petunias, but not to tomato.

Biology. As Liriomyza langei was synonymized with L. huidobrensis until relatively recently, and the latter has become of global significance, little direct work on the biology on the former has been reported. Given prior confusion over the status of L. langei and L. huidobensis, however, studies conducted in the USA on L. huidobensis were likely made on L. langei.

While no assumptions can be made about specific aspects of the leafminer from the information available to date, the general life cycle biology of L. langei is similar to the biology of the major polyphagous Liriomyza species. Female leafminers feed on plant sap by making punctures in the leaves with their ovipositor; they also lay eggs in leaves via punctures made in the same way. The eggs hatch after 2–4 days and larvae mines in the spongy mesophyll of the lower leaf surface; the serpentine mines are usually associated with the midrib and lateral veins. Frick (1951) states that the larval mine is quite wide in this species, being almost twice the larval width for most of the length of the mine. The larvae emerge from the mines and pupate on the leaf surface, or more commonly, in cracks in the soil. The leafminer completes many generations each year and the entire life cycle can be completed in less than three weeks when conditions are warm (Steck and Dixon 2006).

Parrella and Bethke (1984), working in California on the leafminer (as “L. huidobrensis”), found that larval development time was shorter on Pisum sativum than on Chrysanthemum or aster. No differences were found in the duration of the egg or pupal stages or on adult longevity on the three hosts. The largest number of pupae per female and the highest survival rate of pupae were those reared on pea. In addition, Reitz and Trumble (2002) found that Californian populations to have higher reproductive success on pea compared with other hosts.

Movement & Dispersal. There is no readily published information on dispersal, but as the general biology of species is very similar to that of other polyphagous Liriomyza species, dispersal mechanisms are likely to be similar: natural dispersal by flight over limited distances that may be facilitated by wind and broader human facilitated travel via horticulture and ornamental flower trades.

Management. Early detection. Given the pest status of Liriomyza langei in California and its possible movement within the USA via the horticultural trade, a pest alert has been produced for Florida by the Florida Department of Agriculture and Consumer Services (Steck and Dixon 2006). Heinz and Chaney (1995) provided a sequential sampling plan for the estimation of larval populations of this species (as Californian “L. huidobrensis”) and mining damage on celery.

Control. The effects of vacuum and controlled atmosphere treatments on L. langei mortality for lettuce production are summarized by Liu (2003). On host plant resistance, Mou and Ryder (2003) report on experimental work in California where several lines of lettuce and spinach resistant to attack by L. langei were identified. Although no line was completely immune, the trait for ‘resistance’ proved stable and thus provided the potential for crop improvement. Further work is described by Mou and Ryder (2010) on a green lettuce line resistant to leafminer and lettuce mosaic virus that was adapted to major lettuce production areas of the central coast of California. Shi and Mou (2016) evaluated 300 USDA spinach lines for resistance to L. langei and identified five molecular markers potentially of use by plant breeders. Early attempts at control on asters, Lactuca sativa, Spinacea oleracea and Beta vulgaris in the 1950s and 1960s included the insecticide parathion (Jefferson and Eads 1952; Wilcox and Howland 1955), and for B. vulgaris, phorate (Duffus and McCalley 1964). The organophosphate, methamidophos, was reported as being effective for control (Parrella and Keil 1985). Liriomyza langei, however, may have developed strong resistance to a broad range of insecticides (for example, see Steck and Dixon 2006) that mirrors the situation with other polyphagous Liriomyza species (Parrella and Keil 1984) but this remains to be shown experimentally. There is no published work known by the authors on the efficacy of modern products such as insect growth regulators, which are suggested as being effective by Reitz et al. (2013) for other Liriomyza species in general. In Hawaii, attempts to control the leafminer on onions by planting bean borders to boost local parasitoid populations were not successful (Johnson and Mau 1986). Chow and Heinz (2005, 2006) reported on experimental studies using L. langei as a model system, and on improved rearing techniques to avoid male-biased sex ratios for the hymenopterous parasitoid Diglyphus isaea (Eulophidae) in semi-protected field production of Chrysanthemum in Texas; D. isaea is one of the few parasitoids produced commercially for leafminer control ((Chow and Heinz 2004). Likewise, Bader et al. (2006) used a similar system in Texas to study the feasibility of producing a marketable crop using parasitoid species alone or in combination, specifically, D. isaea and D. sibirica (Braconidae). Interspecific competition between the species was undetectable at leafminer densities typical of field grown Chrysanthemum, and release of both parasitoids simultaneously produced no positive benefits.

“Vegetable Leafminer”

(Figs 81–86)

Other Common Names. Serpentine vegetable leafminer, cabbage leafminer, tomato leafminer (CABI & EPPO 2015c).

Identification & Diagnosis. Liriomyza sativae is highly variable in adult morphology and superficially similar to many other species, making male dissection necessary for confident identification. Comparison to published molecular sequence data might be required, especially for larvae or females – see Amin et al. (2014) and Nakamura et al. (2013) as examples. The variation in adult morphology may be due, in part, to the presence of deeply divergent mitochondrial lineages, suggestive of the possibility of cryptic species (Scheffer and Lewis 2005), but much remains to be resolved.

Like almost all other Liriomyza, adult L. sativae has the thorax mostly black dorsally with the shoulders (notopleuron + postpronotum) and centre of the scutellum yellow (Fig. 81). Furthermore, wing length is 1.3–1.8 mm, the pleuron and femora are variably light to dark, the surface of the thorax is very lightly dusted with pruinosity, and the posterolateral corners of the frons around the base of the vertical setae are usually brown to black; while these states are also seen in other Liriomyza, these differentiate it from the common plant pest L. trifolii (Fig. 87), which is similar in size (1.2–1.9 mm), but has an almost entirely yellow pleuron, entirely yellow femora, a denser grey dusting of pruinosity and an entirely yellow frons with only the ocellar tubercle brown.

The male genitalia of Liriomyza sativae are most diagnostic: the surstylus has only one spine (Fig. 83); the mesophallus is slender and separate from the distiphallus; the distiphallus is small, slender and cup-shaped, and in profile, a weak C-shape is apparent due to deeper sclerotization of the apical, basal and ventral surfaces (Figs 85, 86). Although quite similar to the distiphalus of L. trifolli (Figs 90, 91), a related species, the phallus of L. sativae differs in being more rounded and robust, the distiphallus and mesophallus are separate, and the distiphallus venter is thicker and darker (best seen laterally).

Larvae are typically maggot-shaped, and the posterior spiracles are on subconical projections with three bulbs, two of which are elongate (Spencer 1973: fig. 325).

Distribution. Described from Argentina in the 1930s, populations were also found in California at about the same time, suggesting an original widespread distribution spanning the American continents. Liriomyza sativae has been found throughout the New World as far north as California, Colorado and Maryland in the United States. Specimens have also been found in greenhouses north to Maryland, Ohio and Pennsylvania and Ontario (CABI & EPPO 2015c; Lonsdale 2011). This species is often common in growing regions within its range. In tropical and sub-tropical regions, the leafminer mostly occurs in lowland areas (Andersen et al. 2002).

Additional invasive populations occur in the Afrotropical, Australian, Oriental and Palaearctic Regions (CABI 2014; CABI & EPPO 2015c; EPPO 2014; Dempewolf 2004; Lonsdale 2011; Scheffer and Lewis 2005):

•Afrotropical Region: Cameroon, Kenya, Nigeria, Oman, Sudan, Yemen, Zimbabwe. Likely not present in Democratic Republic of Congo, Ethiopia, South Africa or Tanzania.

•Australian Region: Australia (Torres Strait) (Blacket et al. 2015), Cook Islands, French Polynesia, Guam, Micronesia, New Caledonia, Northern Mariana Islands, Papua New Guinea (Blacket et al. 2015), Samoa, Tahiti, Vanuatu, USA (American Samoa, Hawaii). Eradicated from Australia (Queensland).

•Nearctic Region: Canada (Ontario – greenhouse), Mexico, USA (Texas to California, Colorado and South Carolina; in glasshouses in Ohio, Maryland and Pennsylvania).

•Neotropical Region: Antigua and Barbuda, Argentina, Bahamas, Barbados, Brazil (Ceará, Paraná, Pernambuco, Rio de Janiero), Chile, Colombia, Costa Rica, Cuba, Dominica, Dominican Republic, French Guiana, Guadeloupe, Jamaica, Martinique, Montserrat, Netherlands Antilles, Nicaragua, Panama, Peru, Puerto Rico, St. Kitts and Nevis, St. Lucia, St. Vincent and Grenadines, Trinidad and Tobago, Venezuela. Likely absent from Suriname.

•Oriental Region: Bangladesh, China (Fujian, Guangdong, Yunnan), India (Uttar Pradesh), Indonesia (Java), Japan (Ryukus), Malaysia (Peninsular Malaysia), Philippines, Sri Lanka, Thailand, Vietnam. Likely absent from Cambodia, Laos, Pakistan.

•Palaearctic Region: Arabian Peninsula, China (Anhui, Beijing, Hainan, Hebei, Henan, Hunan, Shandong, Shanghai, Shanxi, Sichuan, Xinjiang, Zhejiang), Egypt, Greece (Deeming 2006), Israel, Japan, Jordan, Russia, Turkmenistan, Uzbekistan. Likely absent from Europe, with restricted populations in Turkey.

Hosts. Liriomyza sativae is a highly polyphagous leafminer recorded from 32 families, including many agricultural crops (Lonsdale 2011): Amaranthaceae, Apiaceae, Asteraceae, Begoniaceae, Boraginaceae, Begoniaceae, Capparaceae, Caryophyllaceae, Chenopodiaceae, Cucurbitaceae, Datiscaceae, Dioscoreaceae, Euphorbiaceae, Fabaceae, Lamiaceae, Liliaceae, Malvaceae, Moringaceae, Oleaceae, Onagraceae, Passifloraceae, Plantaginaceae, Poaceae, Polemoniaceae, Polygonaceae, Ranunculaceae, Sapindaceae, Scrophulariaceae, Solanaceae, Tropaeolaceae, Verbenaceae, Zygophyllaceae. Fabaceae, Cucurbitaceae and Solanaceae appear to be most preferred (Spencer 1973).

Damage. Liriomyza sativae is one of the world’s most damaging agromyzid pests, being both highly polyphagous and highly invasive. With heavy leafmining there may be serious damage to numerous important vegetable crops and ornamental plants, principally those in preferred plant families (see above), including tomato (Solanum lycopersicum), beans, melons, cucumber (Cucumis sativus), Pisum sativum and Chrysanthemum (CABI 2015c; Hofsvang et al. 2005; Waterhouse and Norris 1987; Xie et al. 1997).

Damage is caused in several ways (Parrella 1987): destroying young seedlings, reduction in crop yields, leaf damage of ornamental plants and vectoring disease (for the last see Zitter et al. 1977). Tomato plants can tolerate a reasonable amount of mining damage without affecting yield (Levins et al. 1975; Parrella 1987) but young plants are highly susceptible (Hofsvang et al. 2005). Most damage is caused by the developing larvae feeding within mines, but feeding punctures on leaves made by females have been shown to cause a reduction in the vigour of plants; e.g. a reduction of photosynthesis rate in tomato (Johnson et al. 1983).

Biology. Mating usually occurs in daylight hours and within one day of emergence. The female ovipositor is used to puncture the dorsal surface of leaves, producing sap that is used for feeding; eggs may also be deposited within some of these punctures. Egg-laying starts about a day after emergence, peaks after one week and then continues at a lesser rate for a couple of weeks. Several eggs may be laid per leaf, the actual number depending on the type of host plant. Larvae feed within the mesophyll layer, producing a mine shape that is variable, but often broadly linear to serpentine. The third-instar larva exits the mine by cutting an opening at the end of the mine, subsequently pupating on any surrounding foliage or by dropping to the ground and pupating in the upper surface of the soil (Parkman et al.1989; Petitt and Wietlisbach 1994; Spencer 1989; Waterhouse and Norris 1987).

Duration of the developmental stages depends on host plant and temperature: in general, the egg stage lasts 2–5 days and larvae last 4–7 days above a mean temperature of 24°C. The entire life cycle (egg to adult) takes from less than 3 weeks to more than nine weeks (CABI & EPPO 2015c; Pettit et al. 1991); or 250 day-degrees (DD) above a threshold of 10.2°C (Haghani et al. 2007). The mortality rate of immature stages rises significantly above 30°C. On cucumber, the highest intrinsic rate of natural increase (r_m) and net reproductive rate (R₀) were obtained at 25°C (Haghani et al. 2006). In the tropical mountain region of central Java, Indonesia, temperature was found to play an overriding influence on the distribution of L. sativae and a competing species, L. huidobrensis; the former was not found above 1200 m where the average temperature was 20.7°C (Tantowijoyo and Hoffmann 2010).

Movement & Dispersal. The adult is capable of natural dispersal by flight but this is likely only effective over limited distances (EPPO 2015; Parrella 1987). For polyphagous Liriomyza species in general, Parrella (1987) notes that prevailing winds influence the rate and direction of dispersal but in a study with yellow sticky traps, Tryon et al. (1980) noted that catches of L. sativae declined when wind gusts exceeded 20 mph. A study also using yellow sticky traps showed that adult flies were more active in the middle height of tomato plants (Zehnder and Trumble 1984).

The main factor known to influence long distance dispersal has been human activity through the development of an extensive global trade in horticultural and ornamental plants, especially flowers (Parrella and Keil 1984). The presence of extensive greenhouse networks in northern China, which allows the overwintering of pupae, is facilitating the spread of this species further north (Chen and Kang 2005).

Management. Early detection. Information on the global distribution is available via the CABI Invasive Species Compendium (CABI 2015c) and several fact sheets are available on the internet such as CABI & EPPO (2015c). Liriomyza sativae is listed as a major quarantine pest in many regions of the globe. For example, EPPO recommends that propagation material (except seeds) of a defined list of vegetable and ornamental plants from countries where L. sativae is known to occur be inspected at least monthly for three months and shown to be pest free. In addition, a phytosanitary certificate should be required for cut flowers and for harvested and transported vegetables with leaves (OEPP/EPPO 1990).

Sticky traps have been used in the field to monitor adult fly activity and numbers, with yellow traps being more effective than those of other colours (CABI 2015c; Chandler 1981; Tryon et al. 1980). Johnson et al. (1980c) recommended the collection and counting of puparia in trays placed beneath tomato plants to monitor populations of L. sativae. Zehnder and Trumble (1985) developed sequential sampling plans for tomato crops using yellow sticky traps for adult flies and trays for pupal populations; for the former, the authors provided the minimum number of traps that must be counted to estimate various mean densities of adult flies with given levels of precision.

Control. Maintaining general hygiene within horticulture and ornamental flower farms by clearing debris and treating soil to destroy pupae has been suggested by Velez et al. 1980. Some success has been obtained by placing yellow sticky traps close above plants for trapping males as it is suggested that this reduces the number of sexually active males (CABI 2015c). Some authors have reported varietal resistance in tomatoes but this technology has not been adopted commercially. Liriomyza sativae, like other polyphagous Liriomyza, are classic secondary pests (Parrella and Keil 1984; Reitz et al. 2013). The indiscriminate use of insecticides from the 1950s against other pests generated the first outbreaks of Liriomyza leaf miners in the USA, and the situation was exacerbated by the direct use of insecticides against Liriomyza. The effects were twofold: the development of resistance within fly populations and the reduction of natural enemy populations due to greater susceptibility (Waterhouse and Norris 1987). Nonetheless, insecticides are necessary where biological and other controls cannot keep leaf miners below economic thresholds, and much research has focused on new groups of insecticides and their compatibility with parasitoids. Cyromazine (an insect growth regulator) is currently considered to be one of the most effective available products, along with neurotoxins such as abamectin, spinosad and other spinosyns (Reitz et al. 2013), but it is likely that these only remain effective where there is no excessive spraying or concentration of other insecticides (Mason et al. 1989). These products are more compatible with parasitoids than carbamates, organophosphates or pyrethroids (Reitz et al. 2013), but abamectin and spinosad have been shown to be more toxic to parasitoids than cyromazine (Hossain and Poehling 2006). Liriomyza species vary in their susceptibility to different insecticides; e.g. L. sativae is more susceptible to cyromazine than L. trifolii in China (Gao et al. 2012). Research continues on potential biological control agents with most studies and practices to date focusing on hymenopterous parastoids (Liu et al. 2009). Parasitoid communities are diverse, both in North America (e.g. Schuster et al.1991; Schuster and Wharton 1993) and in countries where the pest has been introduced; a summary is provided by Murphy and LaSalle (1999). Observations suggest that parasitoids tend to be habitat/host plant specific rather than leaf miner specific. While Johnson et al. (1980b) showed in a study on pole tomato in California that parasitoids can control L. sativae in the absence of insecticides, few other practical biocontrol programmes have been conducted on field vegetable crops. One of the most notable is the programme of parasitoid introductions into Hawaii and other Pacific Islands in the 1970s, where successful control was achieved by Ganaspidium utilis Beardsley (Eucoilidae) and Neochrysocharis diastatae (Howard) (Eulophidae) (Johnson et al. 1993). Early efforts were made at control in glasshouses by using inoculative releases of Diglyphus species (Eulophidae).

(Figs 49–54)

Identification & Diagnosis. Like other Liriomyza, L. strigata has a black notum with the shoulders (postpronotum+notopleuron) and a medial stripe on the scutellum yellow (Figs 49, 50). Wing length is 1.8–2.2 mm. The phallus is similar to that of the related pests L. huidobrensis and L. bryoniae, where there is a long membranous space between the pigmented section of the ejaculatory duct and the mesophallus, and the distiphallus is small and entirely divided medially, consisting of two short, pigmented tubules. The cup-like tubules of the distiphallus in L. strigata (Figs 53, 54) are broader, however, similar to those of L. bryoniae (compare to Figs 47, 48), but the segment is slightly longer with a longer, wider base, and it is somewhat better sclerotized. Externally, it differs from relatives in having the brown stripe behind the eye reach, or nearly reach, the base of the outer vertical seta (Fig. 51; stripe usually wider in L. huidobrensis and nearly absent in L. bryoniae), the first flagellomere is yellow (infuscated in L. huidobrensis), the anepisternum has a small to well-developed ventral spot/stripe (smaller in L. bryoniae, larger in L. huidobrensis), the katepisternum has a small ventral spot not reaching the base of the katepisternal seta (reaching seta in L. huidobrensis), the femora are yellow with light dorsal streaking (more extensive in L. huidobrensis) and there are 4 rows of acrostichal setulae (usually less in the other species).

The larval posterior spiracle has 10–12 pores across a wide, shallow, semicircular lobe. While morphological identification of males is possible following dissection, differences are slight, and female and immature stages are character poor. As such, molecular methods of differentiation are recommended (see Kox et al. (2005)) when possible following initial morphological screening of adult males, as is the comparison of leaf mines.

Distribution. The distribution of this species is relatively well known in Europe and central Asia (Spencer 1976; Deeming 2006; Martinez 2013), but its presence from eastern Europe to the eastern Palaearctic requires further study, as it is possibly quite widespread. Dempewolf (2004) mentions specimens identified as L. strigata from the Oriental and possibly eastern Palaearctic Regions in India, Malaysia, Singapore and China that require verification. It appears to be absent from Japan, which is relatively well-sampled for Agromyzidae.

•Palaearctic Region: Albania, Belarus, Belgium, Bosnia and Herzegovina (Jovanovic and Dimic 1980), Czech Republic, Denmark, Estonia, Finland, France, Germany, Greece, Hungary, Iraq, Ireland, Italy, Kazakhstan, Kyrgyz Republic, Lithuania, Netherlands, Portugal (Madeira Isl.), Norway, Poland, Romania, Russia, Slovakia, Spain, Sweden, Switzerland, Turkey, Ukraine, United Kingdom, Uzbekistan.

Hosts. Liriomyza strigata is a highly polyphagous leafminer that has been recorded from more than 200 genera of host plants in 35 families (Benavent-Corai et al. 2005), with the addition of Polemonium L. by Edmunds (2008) and Cistus by Ostrauskas et al. (2003): Acanthaceae, Alliaceae, Amaranthaceae, Apiaceae, Araliaceae, Asteraceae, Boraginaceae, Brassicaceae, Campanulaceae, Cannabaceae, Capparaceae, Caryophyllaceae, Celastraceae, Chenopodiaceae, Cistaceae, Convolvulaceae, Cucurbitaceae, Dipsacaceae, Euphorbiaceae, Fabaceae, Hydrophyllaceae, Lamiaceae, Linaceae, Loasaceae, Malvaceae, Papaveraceae, Plantaginaceae, Polemoniaceae, Primulaceae, Resedaceae, Scrophulariaceae, Solanaceae, Tropaeolaceae, Valerianaceae, Verbenaceae, Violaceae.Most hosts belong to the families Asteraceae (76 genera) and Brassicaceae (32 genera). Species of Asteraceae, Campanulaceae and Lamiaceae are preferred (Spencer 1976).

Damage. Liriomyza strigata is a widespread species often encountered on food crops, and while it usually causes little appreciable damage, its potential to develop to pestiferous levels make it significant (Spencer 1973). The species also occurs on a number of ornamentals, where the conspicuous mines could reduce economic value. Its overlap in host preference and morphology with other highly injurious taxa such as L. huidobrensis and L. bryoniae will likely confuse identification and subsequent control measures, and care must be taken during diagnosis.

Biology. Spencer (1973) mentions that ‘surprisingly no detailed studies have been made of the life history of this species’ and this still seems to be the case. According to very early work summarized in Spencer (1973), an adult female lays an egg near the margin of the leaf where the young larva then mines the lower surface until it reaches the midrib, at which point it switches to mining the upper surface. Here the main mines are formed, which are short, straight or irregular offshoots laterally along the veins (Spencer 1973: figs 502, 514; Dempewolf 2004). This is similar to some L. huidobrensis, but in contrast to the irregular serpentine mines formed by L. bryoniae, which can be much more difficult to differentiate as an adult. Pupation is external.

Movement & Dispersal. Published data are not available.. The horticultural trade in host flowers and vegetables will likely aid in this species’ dispersal but this has not been confirmed.

Management. Early detection. Populations of the leafminer are monitored in glasshouses in France by the use of yellow pans (Villevielle 1987). Some of the information given for L. sativae and other polyphagous leafminers may be of relevance for L. strigata.

Control. In glasshouses in Lithuania, trials with the neurotoxin abamectin have been shown to be effective for control of larvae, but similar trials with the neem-based insect growth regulator azadirachtin were not (Duchovskienė & Survilienė, 2009). A wide range of local species of parasitoids (Hymenoptera: Chalcidoidea) have been recorded from Western Europe, as reviewed in (Spencer 1973). More recent records include those from several Liriomyza species in greenhouses in southern Spain, where Neochrysocharis formosa (Westwood) (Eulophidae) was found to be most common, causing parasitism levels of 51% on tomatos, 31.4% on eggplants, and 31.2% on green beans (Phaseolus vulgaris) (Cabello et al. 1994). Similar local parasitoid diversity has been recorded from the field in Turkey (Uygun et al. 1995; Gençer,2009); Diglyphus isaea (Eulophidae) was found to be the most common by Uygun et al. (1995).

“American Serpentine Leafminer”

(Figs 87–91)

Other Common Names. Chrysanthemum leafminer; Serpentine leafminer; minador pequeño del frijol (Spanish); mineuse du gerbera (French) (CABI 2015d).

Identification & Diagnosis. Relatively small, pale species 1.2–1.9 mm (wing length) (Fig. 87). Similar in appearance to many Liriomyza, L. trifolii has a black notum with the shoulders (postpronotum+notopleuron) and the medial stripe on the scutellum yellow, but the scutum is covered with a greyish pruinosity and there are usually only two rows of acrostichal setulae (but sometimes up to four). The femora are yellow, but sometimes with very limited brown spots, the abdomen is broadly yellow laterally and the pleuron is relatively pale with a spot on the katepisternum and very limited brown mottling on the anepisternum. The head is especially diagnostic among pestiferous Liriomyza in that the frons is entirely yellow, including the posterolateral region around the base of the vertical setae, but the ocellar tubercle remains brown; the antenna (excluding arista) is entirely yellow with the first flagellomere sometimes slightly pointed anterodorsally.

The male genitalia are characterized by a pale, slender phallus with a small cup-like distiphallus fused to a very narrow mesophallus (Figs 90, 91), and the surstylus has only a single spine (Fig. 88).

Minor variations across specimens of Liriomyza trifolii may be indicative of the presence of cryptic sister species exhibiting restricted host preference, as suggested by analyses of mitochondrial sequence data (Scheffer and Lewis 2006; Pérez-Alquicira et al. 2019).

Larvae are typically maggot-shaped and indistinguishable from those of Liriomyza sativae (Spencer 1973).

Distribution. Liriomyza trifolii is native to the New World, possibly with origins in the Neotropics, although the phylogeography of this species is yet to be confidently resolved. The ability of this species to disperse and colonise following human-mediated transport is considerable (Minkenberg 1988a). Interceptions via trade are frequent, especially on Chrysanthemum, resulting today in a wide global distribution (Lonsdale 2011; Černý and Tschirnhaus 2014; EPPO 2014; CABI & EPPO 2015d). Aside from known occurrences, this species is likely present but undetected in many additional localities, including the lower 48 states in the USA and all Mediterranean countries (CABI 2015d). Additional focused sampling in Africa, Oceania and central, east and southeast Asia is required for better global estimates.

Populations appear to be less common in northern Canada, Europe and Asia where they are unable to overwinter, but may be sustained in glasshouses. South temperate countries and Australia may be similarly restricted or less ideal for development.

•Afrotropical Region: Angola, Benin, Cameroon (Duclaire et al. 2014), Cote d’Ivoire, Ethiopia, France (Mayotte), Guinea, Kenya, Madagascar, Mauritius, Mayotte, Nigeria, Oman, Réunion, Senegal, South Africa, Sudan, Tanzania, Yemen, Zambia, Zimbabwe.

•Australian Region: Australia (northern WA, northern QLD (IPPC 2017)), Guam, Micronesia, Northern Mariana Islands, Samoa, Tonga, USA (American Samoa, Hawaii).

•Nearctic Region: Canada (Alberta, Nova Scotia, Ontario, Prince Edward Island, Quebec), USA (Arizona, California, Delaware, District of Columbia, Florida, Indiana, Iowa, Maryland, Massachusetts. Michigan, New Jersey, New Mexico, New York, Ohio, Oregon, Pennsylvania, South Carolina, Texas, Utah, Washington, Wisconsin).

•Neotropical Region: Argentina, Bahamas, Barbados, Bermuda, Brazil (Minas Gerais, Pernambuco, São Paulo), Chile (Juan Fernandez Islands), Colombia, Costa Rica, Cuba, Dominican Republic, Ecuador, French Guiana, Guadeloupe, Guatemala, Guyana, Martinique, Mexico (states unknown – Mexican specimens recovered in exported plant products), Netherlands Antilles, Peru, Puerto Rico, St. Kitts-Nevis, Trinidad & Tobago, Venezuela, Virgin Islands (British, US).

•Oriental Region: China (Fujian, Guangdong), India (Andhra Pradesh, Delhi, Gujarat, Haryana, Karnataka, Kerala, Madhya Pradesh, Maharashtra, Orissa, Punjab, Tamil Nadu, Uttar Pradesh, West Bengal), Philippines, Taiwan, Vietnam. Likely absent in Cambodia, Malaysia and Thailand.

•Palaearctic Region: Austria, Belgium, Bosnia & Herzegovina, China (Hainan, Jiangsu), Croatia, Cyprus, Egypt, Finland (occasional glasshouse occurrences), France, Greece, Iran, Israel, Italy, Japan, Jordan, Korean Republic, Lebanon, Malta, Netherlands, Portugal, Romania, Russia, Saudi Arabia, Serbia, Slovenia, Spain, Switzerland, Tunisia, Turkey, United Arab Emirates. Considered eradicated from Bulgaria, Czech Republic, Denmark, Estonia, Germany, Hungary, Ireland, Norway, Poland, Slovakia, Sweden, and United Kingdom.

Hosts. Liriomyza trifolii is a highly polyphagous leafminer that has been recorded from many host plant species in 41 families (Benavent-Corai et al. 2005), including: Acanthaceae, Amaranthaceae, Anacardiaceae, Apiaceae, Asclepiadaceae, Asteraceae, Basellaceae, Begoniaceae, Campanulaceae, Capparaceae, Caryophyllaceae, Chenopodiaceae, Convolvulaceae, Cucurbitaceae, Euphorbiaceae, Fabaceae, Goodeniaceae, Iridaceae, Lamiaceae, Liliaceae, Malvaceae, Onagraceae, Passifloraceae, Piperaceae, Plantaginaceae, Poaceae, Polemoniaceae, Polygonaceae, Portulacaceae, Primulaceae, Ranunculaceae, Rosaceae, Sapindaceae, Scrophulariaceae, Solanaceae, Tropaeolaceae, Turneraceae, Typhaceae, Valerianaceae, Verbenaceae, Zygophyllaceae.

Major hosts are found among the 50 genera of Asteraceae known to be attacked (see Lonsdale (2011)), including Helianthus L. and Lactuca L., as well as numerous ornamentals including Aster L., Bidens, Dahlia, Gerbera L., Tagetes L. and especially the commercially important Chrysanthemum. Affected crops in other families include beets (Beta vulgaris), carrot (Daucus carota sativus (Hoffm.) Schübl. & G.Martens), celery (Apium graveolens), peppers (Capsicum), cotton (Gossypium), onions (Allium cepa L.), leek (A. ampeloprasum), garlic (A. sativum), oat (Avena sativa L.), barley (Hordeum), melons, okra (Abelmoschus esculentus), potato (Solanum tuberosum), spinach (Spinacia oleracea), tomato (Solanum lycopersicum), Senecio L., Gypsophila, Brassica, and many Fabaceae including clover, soy and many beans and peas (Lonsdale 2011; CABI 2015d).

Mitochondrial sequence data has found that L. trifolii feeding on Capsicum sp., Physalis philadelphica Lam. and possibly Apium graveolens together form a clade that is distinct from L. trifolii feeding on other sampled hosts, suggesting the presence of a cryptic species with a relatively restricted host range (Scheffer and Lewis 2006; Pérez-Alquicira et al. 2019). This is consistent with previous findings of a pepper-adapted population in central California (Morgan et al. 2000; Reitz and Trumble 2003). Considerably more sampling of L. trifolii from additional hosts and locations, for both molecular and morphological analysis will be necessary to better understand host-use and population structure in L. trifolii.

Damage. This leafminer is an important pest of many vegetable crops and ornamental flowers (CABI 2015d). Damage manifests in several ways - feeding punctures cause ‘stippling’ and a reduction in the quality of crops and ornamentals; leafmining larvae delay development or destroy young seedlings; older plants exhibit leaf drop and/or yield loss; plants are exposed to infection by pathogenic fungi; transmission of plant viruses (CABI 2015d; PaDIL 2016; Parrella 1987). On bell pepper (Capsicum annuum) in Texas, USA, the number of mines per plant was not a good indicator of the total damage to the plant (Chandler and Gilstrap 1987).

Economic losses have been considerable. In California, the species caused a loss of US$93m to the Chrysanthemum industry over five years in the early 1980s (Parrella 1987) and losses to celery of US$9m in Florida in 1980 (Foster and Sanchez 1988).

Biology. Adult flies mostly emerge before midday and mating usually takes place within 24 hours (CABI 2015d). Females puncture leaves for both feeding and egg laying, with approximately 15% of punctures containing eggs (Parrella et al. 1981). The larval feeding produces a linear upper-surface mine; the larva exits the mine from the upper epidermis to pupate in the soil (Eiseman and Lonsdale 2018). The particular biological characteristics (e.g. feeding punctures, viable eggs) of L. trifolii vary according host plant species, with Parrella et al. (1983) finding that the ratio of fertility to feeding punctures per female was greatest on Chrysanthemum, followed by celery and then tomato. Many studies of the life history of L. trifolii have been conducted on tomato as host; using yellow sticky traps Chandler (1985) and Zehnder and Trumble (1984b) showed that adult flies are more active in the lower part of tomato plants.

The development times of each life stage have been reported by several authors; Minkenberg (1988b) studied development at a number of constant and fluctuating temperatures on tomato. At 15 and 25°C, the duration in days of the immature stages was, respectively: egg 6.6 and 2.7; first star larva 3.3 and 1.4; second instar larva 3.7 and 1.4; third instar larva 3.7 and 1.8; and pupa 26.8 and 9.3; total development time at the two temperatures were 44.0 and 16.6 days, respectively. At these temperatures, the intrinsic rates of increase (r_m) were -0.0023 viable female eggs per female per day to 0.1254 eggs per female per day. The development threshold is 9.7°C and development in degree-days (egg to adult) is 564.7 (UC IPM 2015). Leibee (1984) found that the maximum oviposition rate of 38.67 eggs per female per day and fecundity of 405.67 eggs per female were at 30°C.

In the southern USA, breeding is likely to be throughout the year (CABI 2015d). In the UK, pupae remain viable outdoors for several months and can tolerate freezing temperatures (Millar and Isger 1985).

Movement & Dispersal. Natural dispersal by flight is probably only over limited distances (Parrella 1987) and in horticultural crops, adult flies remain close to the crops (Zehnder and Trumble 1984a). In Chrysanthemum greenhouses, Jones and Parrella (1986) found that on average, females fly further than males and that density decreased (from the release point) more rapidly for the latter than the former. Parrella (1987) notes that prevailing winds influence the rate and direction of dispersal of Liriomyza species, and it has been suggested that agromyzids can travel long distances aided by wind (PaDIL 2016). However, of more importance in long distance dispersal of L. trifolii is the global development of the extensive horticulture and ornamental flower trades (Parrella and Keil 1984).

Management. Early detection. Up-to-date information on global distribution is available via the CABI Invasive Species Compendium (CABI 2015d). Risk assessments covering key features of the biology of the leafminer, pathways of movement and methods of identification have been produced for Europe (EFSA Panel on Plant Health 2012) and Australia (PaDIL 2016). Adult flies can be monitored in the field using sticky traps, with yellow traps performing better than other colours (CABI 2015d; Chandler 1981). A sequential sampling plan using yellow traps has been developed to estimate adult populations in Chrysanthemum greenhouses, but the technique has limited value in predicting immature stages (Parrella and Jones 1985). Sequential sampling plans have also been developed for tomato crops, using yellow sticky traps and trays to estimate populations from adult and pupal stages, respectively (Zehnder and Trumble 1985). Yellow sticky traps have also been used to monitor insecticide resistance in Liriomyza trifolii populations (Sanderson et al. 1989).

Control. Sanitation methods, including the removal of crop plant residues and the deep burying of old weeds, are recommended as these can still be infested with the leafminer. Sticky traps have been effective in controlling adults in onion crops in the Philippines, with yellow traps performing better than other colours (Arida et al. 2013). Chrysanthemum cuttings should be maintained in glasshouses for 3–4 days after lifting to allow all eggs to hatch, followed by storage at 00C for 1 to 2 weeks to kill larvae (CABI 2015d). Kapsey and Parrella (2006) also suggested the release of sterile male flies to improve biological control in glasshouses. Several studies have detected an effect of oviposition deterrence in extracts from mature leaves of Capsicum annuum (Kashiwagi et al. 2005; Dekebo et al. 2007; Tebayashi et al. 2007). Liriomyza trifolii became a major problem on crops and ornamentals because of overuse of insecticides in the second half of the 20^th century (Parrella and Keil 1984; Reitz et al. 2013), mainly through the development of resistance, but also by indirect effects on local natural enemies. In the USA in Florida, the average life of effectiveness of an insecticide was roughly between two to four years (Reitz et al. 2013). Reitz et al.’s (2013) review of insecticides stated that the insect growth regulator cyromazine is currently one of the most effective products for control, but abamectin and spinosyns such as spinosad, which act as neurotoxins, are also effective. However, these will only remain effective where there is no excessive frequency of spraying (Mason et al. 1989) and where different insecticides are rotated on a regular basis (CABI 2015d). Much work has been done on the natural enemies and biological control of L. trifolii, with good reviews provided by CABI (2015), Liu et al. (2009) and Waterhouse and Norris (1987). The leafminer is attacked by a range of natural enemies such as insect predators and entomopathogenic nematodes, fungi and bacteria, but insect parasitoids have been the most exploited agents to date because species are quite common and diverse (Liu et al. 2009). Commonly used parasitoid species include: Diglyphus and Chrysocharis Förster (Eulophidae); Dacnusa and Opius (Braconidae) and Ganaspidium (Cynipidae). Introduction biological control using parasitoids was successful in Hawaii in the late 1970s on watermelon and possibly celery using Ganaspidium utilis. Effective control of the leafminer in Tonga was also achieved using this agent on a range of vegetable crops in the late 1980s, together with Chrysocharis oscinidis Ashmead (Johnson 1993). For the control of the leafminer in glasshouses, inundative releases of Diglyphus isaea and Dacnusa sibirica have been used successfully in Europe and Japan (Liu et al. 2009). For ornamentals, Diglyphus begini (Ashmead) has been used to control the leafminer on marigolds (Heinz et al. 1988). Studies on the more suitable insecticides have shown that abamectin and spinosad are more toxic to parasitoids than cyromazine (Hossain and Poehling 2006).

“Soybean Stem Miner”

(Figs 92–99)

Other Common Names. Asparagus miner; bean stem miner; soy miner; soybean fly; soybean stem borer; soybean fly; soybean stem borer; agromyze des tiges du soja (French) (CABI 2020).

Identification & Diagnosis. Melanagromyza sojae males should be dissected for confident diagnosis. Like many other Melanagromyza externally, it is relatively small with a wing length of 1.7–2.1 mm, there are two dorsocentral setae with the anterior seta slightly smaller, there are four fronto-orbital setae, there are about eight rows of acrostichal setulae, and the calypter margin and hairs are white (Figs 92–94). The body is dark brown to blackish; a minimal greenish or bluish shine is sometimes evident on the notum, and the abdomen is distinctly metallic green. The head of the species is relatively distinct in that the eyes of both sexes are bare (in most Melanagromyza, the dorsal surface of the eye has at least some minute hairs that can be dense and bushy in males of many species), the orbital plate is narrow with only a single irregular row of reclinate setulae, the ocellar triangle is almost shining and long (nearly reaching the anterior margin of the frons), and the gena is highest near the anterior margin. The phallus (Figs 98, 99) has a basiphallus that is as long as, and is adjacent to the phallophorus, and the basiphallus is separated from the distiphallus by approximately its own length. The dorsal chamber of the distiphallus is relatively small, not strongly pointed or extended apically, and is minimally spinulose internally; the ventrolateral tubules emerging from the base of the chamber are quite thick and prominent, looping far basally. The mesophallus is inserted into the dorsal chamber ventromedially near the base of the segment, and extends basally past the chamber, including the ventrolateral tubules. Almost all Melanagromyza have a single spine in the inner posteroventral margin of the epandrium, but it is missing in this species (Figs 96, 97). To differentiate the immatures from other bean flies, the posterior spiracles have a central horn that is highly atrophied (see Spencer (1973: figs 44–46)).

Distribution. Most of the known distribution of this species was summarized by CABI (2020). Since the immature stages occur in the host stem, and the seed and pods are traded internationally, the probability of accidental introduction into other regions is relatively low (CABI 2020). Screening of whole plants for international trade and breeding, however, should be done with care.

•Afrotropical Region: South Africa, Sudan (Abdel-Banat et al. 2017).

•Australian Region: Australia, Solomon Islands.

•Neotropical Region: Argentina (Vera et al. 2020), Bolivia, Brazil (Goiás, Rio Grande do Sul, Santa Catarina (Arnemann et al. 2015)), Paraguay (Guedes et al. 2017).

•Oriental Region: Bangladesh, China (Fujian), India (Bihar (Singh and Ipe 1973), Delhi, Karnataka, Madhya Pradesh, Maharashtra, Nagaland (Longchar et al. 2019), Rajasthan, Uttar Pradesh, Uttarakhand), Indonesia (Java, Sumatra), Laos, Malaysia (Peninsular), Philippines, Taiwan, Thailand, Vietnam.

•Palaearctic Region: China (Heilongjiang (Yang et al. 1994), Jiangsu, Shandong), Egypt, Israel, Japan, Nepal(?), Saudi Arabia, South Korea, Turkey, Spain. Deeming (2006) additionally recorded Bahrain, Saudi Arabia, Oman and Yemen.

Thapa (2012) identified specimens from India and Nepal, but illustrated specimens representing interspecific variability clearly belong to multiple taxa; the phallus of one illustrated male (plate 2) mostly agrees with known morphology.

Hosts. Melanagromyza sojae feeds primarily as a stem miner and is oligophagous, with favored hosts primarily in the Phaseoleae (Spencer 1990). Soybean (Glycine max) is recorded as the most strongly favoured host by CABI (2020). Additional food crops include Chinese clover (Astragalus sinicus L.), pigeon pea (Cajanus cajan), sunn hemp (Crotalaria juncea L.), alfalfa (Medicago sativa L.), common bean (Phaseolus vulgaris), pea (Pisum sativum), adzuki bean (Vigna angularis (Willd.) Ohwi & H. Ohashi), black gram (V. mungo), mung bean (V. radiata), asparagus bean (V. sinensis sesquipedalis (L.) Van Eselt.) and cowpea (Vigna unguiculata) (Spencer 1973; CABI 2020). The species also attacks Indigofera suffruticosa Mill. and I. tinctoria L. (true indigo), which are used as dyes, and wild hosts include Aeschytomene indica L., Flemingia Roxb. ex W. T. Aiton sp. and Swainsona galegifolia (Andrews) R.Br. (see Spencer (1973)). It has recently been reported from Cicer arietinum (Vera et al. 2021).

Damage. Melanagromyza sojae mostly affects soybean but can be a problem on mung bean and black gram. The insect tends to be more of a problem in dry seasons than wet seasons (CABI 2020). Estimates of yield loss vary according to the study and location but in general, on soybean, yield loss decreases in relation to plant age; thus, yield loss is highest in young seedings at the unifoliate or trifoliate stages but the insect rarely results in plant mortality. In Taiwan, yield loss was estimated at 31% from an assessment of attack on 163 soybean varieties (CABI 2020). In Indonesia, despite high levels of infestation, yield loss was found to be minimal under either early or late stage of plant attack by the fly (van den Berg et al. 1998). However, in Egypt, Alfy et al. (2019) mention yield losses of nearly 100%. Pozebon et al. (2021) did not quantify damage incurred from the species in South America crops where populations are rapidly spreading, but mentioned that in Rio Grande do Sul, Brazil, 95–100% of plants in all second season soybean crops surveyed incurred damage along the length of the plant stem.

Biology. The following is summarized from CABI (2020) and Spencer (1973) with additional information added where relevant. Adults mostly emerge in the early hours of the day. Females puncture the upper surface of leaves of a host plant for feeding; in Taiwan, the adults live 6–19 days (Wang 1979). The eggs are laid in the undersides of leaves, usually near the leaf base. Normally, only one or two eggs are laid per leaf but more may be laid at high adult population densities. After hatching, the young larvae enter the nearest leaf vein and then tunnel through the petiole to the stem pith and then downwards to the top part of the taproot. If not fully developed, the larvae move back up the stem until ready to pupate. They pupate deep within the stem but before doing so, they create a tunnel to the epidermis to allow the subsequent adult to escape.

In Taiwan, the eggs take from 2–7 days to hatch with a peak at 3 days (Wang 1979). There are three larval instars and the total development time at 32±2°C and 70% RH was seven days. The natural mortality of the larvae is quite high with 62% in the first instar, and 24 and 20% in the second and third (Wang 1979). The pupal stage lasts about eight days at 30±2°C and 70% RH. In lowland Indonesia, the total development time from egg to adult is 16–26 days.

Movement & Dispersal. The adults are weak fliers and thus movement is influenced by local weather conditions (CABI 2020).

Management. Early detection. CABI (2020) data sheet provides up to date information on the current global distribution and on likely pathways of spread. The current advice for field monitoring is the same as for Ophiomyia phaseoli (Plantwise 2020).

Control. In many regions in the Old World, Melanagromyza sojae affects the same legumes as another agromyzid, Ophiomyia phaseoli, a species that can be a more serious pest. Given the similar life histories of the two species, the general advice on management of M. sojae is to follow that of Ophiomyia phaseoli (CABI 2019). However, specific information from studies is as follows. Searches for soybean accessions that are resistant to attack by M. sojae have been made in Asia and Africa. For example, Chiang and Talekar (1980) report on accessions of ‘wild soybean’ (Glycine soja Siebold & Zucc.) that are resistant to the insect. However, breeding these into cultivated soybean (Glycine max) was not successful because wild soybean has thin stems which, when expressed in crosses, results in plants that cannot support high pod production. Talekar (1989) suggests that late-maturing soybean cultivars may be less susceptible than early ones. In Egypt, Alfy (2017) found that yellow and white sticky traps suppressed populations in soybean fields. Insecticides are the mostly widely used control method by farmers. Preventative and curative insecticides are recommended although the former is likely to have more impact as most yield loss is at the seedling stage (CABI 2020). In India, the use of a systemic seed dressing (thiamethoxam) along with foliar sprays was found to suppress M. sojae populations in field soybeans (Gotyal and Prasad 2013). Talekar (1990) provides an overview of chemical controls. Studies in several countries in the Old World (India, Indonesia and Taiwan) have shown that M. sojae is attacked by a variety of hymenopterous parasitoids (Beche et al. 2018; CABI 2020). In Maharashta, India, for example, the pest is attacked by ten parasitoids with peak parasitism reaching 50%. Eurytoma Illiger sp. (Eurytomidae) and Gronotoma Förster sp. (Figitidae) were most prevalent throughout the crop season but Sphegigaster Spinola sp. (Pteromalidae), a pupal parasitoid, was the most common mid-season (Fand et al. 2018). A Sphegigaster sp. has been recorded from Egypt where the maximum parasitism recorded was 38.7% (Alfy et al. 2019). Syntomopus parisii De Santis (Pteromalidae) has been recorded as a major parasitoid of the larva and pupa in South America (Beche et al. 2018). In Sumatra, Indonesia, average parasitism reached 60% at the end of crop seasons (van den Berg et al. 1995). In some of these studies the authors suggest that efforts should be made to develop conservation strategies to enhance the impacts of these parasitoids. However, in general, parasitism tends to come late in the crop season and after the pest has done most damage, so such strategies may have little impact on reducing crop losses (CABI 2020).

“Bean Fly”

(Figs 100–105)

Other Common Names. Bean stem maggot. Note that the common name “Bean Fly” is also used to refer to Ophiomyia spencerella and Ophiomyia centrosematis.

Identification & Diagnosis. Ophiomyia phaseoli is a small, completely black species with a wing length of 1.7–2.2 mm (Figs 100, 101). The frons is most diagnostic, being relatively narrow with a finely textured frontal vitta that strongly contrasts a narrow shining orbital plate and a highly polished ocellar triangle; the triangle itself is narrow, sharply delimited and nearly attains the anterior margin of the frons (Fig. 102). Like all Ophiomyia, the anterior margin of the clypeus is truncated, but unlike many congeners it is more broadly U-shaped, and neither it nor the buccal cavity are narrowed (as in Ophiomyia simplex – see Fig. 109). Also contrasting most other Ophiomyia, the narrow gena is not projecting anteriorly, and the facial carina is very shallow and almost indistinct. Other external diagnostic characters include two reclinate positerior fronto-orbitals and two shorter inclinate anterior fronto-orbitals (only anterior seta strongly incurved); two strong dorsocentrals; a costa that extends to vein M₁; a brown to dark brown calypter margin and hairs; and no posterolateral seta on the mid tibia. The male genitalia are also diagnostic, characterized by a H-shaped basiphallus that lies under the ejaculatory duct, and a short, lobate mesophallus that is positioned ventrobasally to a longer, narrow distiphallus that is darker and swollen basally (Figs 103, 104).

Distribution. This species likely occurs throughout the Old World tropics in sub-Saharan Africa, and south and Southeast Asia. Collection records extend north into Oriental China and Japan, and the southern Palaearctic, including northern Africa, Israel, Turkey and Iran. It is additionally known from Australia, Hawaii (widespread – see Hardy and Delfinado (1980)) and Oceania (CABI 2019; EPPO 2019). It is not known from the continental United States (USDA 1984).

•Afrotropical Region: Burundi, Cape Verde Islands (Černý and Tschirnhaus 2014), Congo, Ethiopia, Kenya, Libya, Madagascar, Malawi, Mali, Mauritius, Mozambique (Davies 1998), Nigeria, Oman (Deeming 2006), Réunion, Rwanda, Senegal, South Africa, Sudan, Tanzania, Uganda, Zambia, Zimbabwe.

•Australian Region: Australia (New South Wales, Northern Territory, Queensland, Western Australia), Caroline Island (Waterhouse 1998), Fiji, Guam, Northern Mariana Islands, Palau, Papua New Guinea, Samoa, Solomon Islands, USA (Hawaii [introduced]).

•Oriental Region: Bangladesh, Brunei (Waterhouse 1998), China (Fujian (Shi et al. 2015), Guangdong, Guangxi, Hong Kong), Christmas Island, India (Andhra Pradesh, Andaman and Nicobar Islands (Mitra et al. 2010), Assam, Bihar, Gujarat, Karnataka, Meghalaya, Odisha, Punjab, Rajasthan, Tamil Nadu, Uttar Pradesh, Uttarakhand), Indonesia (Irian Jaya, Java, Sumatra), Japan (Ryukus), Laos, Malaysia (Sabah, Sarawak, Malaya), Myanmar, Pakistan, Philippines, Singapore, Sri Lanka, Taiwan, Thailand, Vietnam.

•Palaearctic Region: Egypt, Iran, Iraq (Deeming 2006), Israel, Jordan, Nepal, Saudi Arabia. Reports of Ophiomyia phaseoli in northern China (Shandong) in Anonymous (1978) are attributable to Melanagromyza sojae (Zehntner).

Hosts. Ophiomyia phaseoli attacks a wide range of leguminous plants (Fabaceae), but is especially damaging to the commonly cultivated bean (Phaseolus vulgaris). Other host species can be highly affected regionally, including soybean (Glycine max) (Bhattacharjee 1980; Arunin 1978), black gram (Vigna mungo) (see Prodhan et al. (2000)), mung bean (V. radiata) (Thapa and Timsina 1990) and pea (Pisum sativum) (Yadav et al. 2019a; Kooner et al. 1977).

Minor hosts include Cajanus cajan, Crotalaria juncea, C. pallida Aiton, Cyamopsis tetragonoloba (L.) Taub., Lablab purpureus, Macroptilium lathyroides (L.) Urb. var. lathyroides, Macrotyloma uniflorum (Lam.) Verdc., Medicago sativa, Mucuna pruriens (L.) DC, Phaseolus coccineus L., P. lunatus, Psophocarpus tetragonolobus (L.) DC, Vigna aconitifolia (Jacq.) Marechal, V. angularis, V. sinensis sesquipedalis and V. unguiculata (Plantwise 2023). Other hosts for which this species has been reared include: Crotalaria laburnifolia L. (Abate 1991), Canavalia ensiformis (L.) DC, Macroptilium atropurpureum (Moc. & Sessé ex DC.) Urb., M. panduratum (Mart. ex Benth.) Maréchal & Baudet, P. acutifolius A. Gray (USDA 1984), P. aurea (Roxb.) Maekawa (Mazumdar and Bhuiya 2014) and V. umbellata (Spencer 1973). Reported occurrence of the bean fly on okra (Abelmoschus esculentus, Malvaceae) in Rai et al. (2014) is in error.

Damage. Ophiomyia phaseoli has proved to be a major constraint on the production of common bean, one of the world’s most import legume crops (Achiri et al. 2021). Oviposition occurs in leaves, stems, and cotyledons, typically of young seedings (Plantwise 2023; Achiri et al. 2021). Punctures made by females can damage the leaves such that photosynthetic rates are reduced with defoliation possible when many punctures are present. The mining of leaf material by young larvae can cause leaves to wilt but the most serious damage is done by later stage larvae that have tunneled downwards through the plant stem and into the top part of the tap root. This can interfere with the transport of water and nutrients and can cause the plant to wilt, weaken and become stunted, sometimes resulting in plant death. Aggregation of puparia within the stem base can also cause it to swell and split (USDA 1984). Damaged plants are likely to have poor pod and seed formation (Nderitu et al. 1990a) and are also likely to break at the soil surface under windy conditions (Greathead 1969). Some plants may respond to attack by developing adventitious roots and, after recovery, are able to withstand further attack (Greathead 1969).

Other host legume species, as well as different cultivars of common bean can show different levels of susceptibility (Ojwang et al. 2010; Tengecho et al. 1988).

In Kenya on common bean, numbers of leaf punctures and eggs peaked at 5–6 weeks after plant emergence, and later plantings in any season had higher infestation levels of bean fly than early plantings (Nderitu et al. 1990a; Songa and Ampofo 1999). The latter was also reported for plantings in Tanzania (Sarah and Makundi 2007). Damage among crops is higher during dry seasons (Abate 1991; Manohar and Balasubramanian 1980; Nderitu et al. 1990b; Plantwise 2023), especially in areas with low soil fertility (Ojwang et al. 2011a). In East Africa, the damage caused to common bean may be exacerbated because of the overlap in distribution with another major damaging similar agromyzid, Ophiomyia spencerella (Greathead 1969).

There is a long history of extensive larval damage to common bean in multiple geographic regions. Crop or plant loss can be total, with examples of 100% seedling loss of late-planted beans in Egypt (Hammad 1978) and 100% crop loss in Western Australia (Morgan 1940). Other reported damage has included 100% plant infestation with 80% seedling mortality in Indonesia (van der Goot 1930), and 100% seedling infestation in Tanzania (Swaine 1968), sometimes with 30–50% yield loss (Wallace 1939). Cultivars of P. vulgaris show differing degrees of resistance to the species (Ssekandi et al. 2016; Tengecho et al. 1988; Rogers 1980), and genetic modification supplementing inherent cultivar resistance in these beans is being investigated (eg. Ojwang et al. 2011b).

In other hosts, Arunin (1978) reported 90% seedling loss in soybean, and Kooner et al. (1977) reported up to 40% mortality and approximately 50% yield loss in pea.

It has been suggested the bean fly further contributes to crop damage via the introduction of root rot at ground level, which can rapidly contribute to yield loss; Athelia rolfsii (Curzi) C.C. Tu & Kimbr., Rhizoctonia solani J.G. Kühn and Fusarium solani (Mart.) Sacc. were all identified in infested plants in Mozambique (Davies 1998).

Biology. Several reviews of the literature are available; the following, where common bean is the host, is summarized from the CABI (2019) and Waterhouse (1998), with additional information added where relevant. Female Ophiomyia phaseoli begin oviposition 3–4 days after emergence and are most active on warm clear days. On bean, they primarily puncture the upper, but sometimes the lower epidermis of leaves or cotyledons with their ovipositors for feeding on plant sap and oviposition. However, only 10–15% of punctures receive an egg. A study on pigeon pea in India found that eggs are always laid on the underside of young leaves and the larvae pupate in the stem (Savde et al. 2018; Yadav et al. 2019). Oviposition can continue for a couple weeks over which 100 to 300 eggs may be laid. The incubation period lasts 2–4 days depending on temperature.

Ophiomyia phaseoli is unusual among miners as the larvae are able to move between tissue types within the plant. The first instar mines along leaf veins towards the mid-rib and in seedlings, the hatched larva forms a narrow, curved mine that is more visible on the underside of the leaf. The second instar feeds mainly in the mid-rib before entering the petiole where it moults into the third instar. This final instar mines down the main stem mostly beneath the epidermis usually to the level of the soil. The fully-grown larva creates a semi-circular hole in the stem epidermis to allow the adult to emerge following pupation. Larvae from eggs laid in leaves in older plants pupate in the main stem below a petiole (Greathead 1969). The total development time on bean depends on temperature: Greathead (1969) found that egg to adult took 27–31 days at about 21°C with a preoviposition of about 2 days.

Fly density in individual bean plants have been reported to be as high as 25 larvae in Egyptian crops, with seedlings beginning to succumb at densities of 10–15 larvae (Hassan 1947). Ethylene production associated with plant stress in the presence of larvae contributes to the production of adventitious roots, as well as the thickening of roots below ground (see Tengecho et al. (1988)); the success of adventitious root development is dependent on moisture availability (Abate 1993).

Movement & Dispersal. The adults are active fliers and most active on warm days (CABI 2019). There is no available information on natural dispersal but CABI (2019) lists the plant parts that are liable to carry the pest in trade and transport.

Management. Early detection. The CABI (2019) data sheet provides up to date information on the current global distribution and on likely pathways of spread. Should the species be accidentally transported to the New World, the threat to bean crops would be severe, although the risk of introduction is lessened by the fact that affected parts of the plant are usually not packaged for export, with the beans themselves being untouched by direct larval damage. Advice includes searching bean crops for small black flies sitting on young leaves and/or evidence of leaf punctures (CABI 2019).

Control. The potential for several generations a year (Avidov and Harpaz 1969), compounded by the ability to accumulate population numbers in a relatively broad spectrum of alternate leguminous hosts, make this species potentially difficult to control. As the bean fly will attack its host crops from the early seedling stage, it is important to act within the first 4–5 weeks after crop emergence. This is particularly important in regions where legume crops such as soybean and mungbean are grown in a dry season following a wet season. Furthermore, as the main damage is hidden within the stem, it is necessary to know the seasonality of the pest in order to judge the timings of interventions (Plantwise 2023). Summaries of management practices are given by Yadav et al. (2019b), Achiri et al. (2021 and in the Plantwise database (Plantwise 2023). Specific information from studies on control are as follows. Cultural controls have been reviewed by Achiri et al. (2021). Ridging crops 2–3 weeks after emergence is suggested to help cover adventitious roots that are sometimes produced by attacked plants. In East Africa, other variously successful practices to avoid severe attacks on common bean include early planting and sanitation (Ssekandi et al. 2016). Effects of planting density and special arrangement, including intercropping, on attack by Ophiomyia phaseoli have been explored with good results (Peter et al. 2009; Achiri et al. 2001); pest populations are lower in mixed cropping systems than in a mono-cropping system (Abate and Ampofo 1996). Cultivars of P. vulgaris show differing degrees of resistance to the species (Ssekandi et al. 2016; Tengecho et al. 1988; Rogers 1980), and genetic modification supplementing inherent cultivar resistance in these beans is being investigated (eg. Ojwang et al. 2011b). Effort has been made by some international research centres and others to develop resistant cultivars (e.g. Ojwang et al. 2010), but in general, research is still ongoing (Nkhata et al. 2021). It is worth noting that in East Africa, there are local preferences by small landholders to grow mixtures of traditional and modern cultivars which they believe provide some resistance to pests and diseases, including the bean fly (Letoureau 1994; Ssekandi et al. 2016), but the effectiveness of this is not known. Insecticides are the mostly widely used control methods in cases where farmers can afford the expense. Given that larvae are hidden is stems, systemics are recommended. Some current recommended advice does not specify specific chemical insecticides because of variable regulations around insecticides from country to country (Plantwise 2023). Studies of natural enemies from several countries indicates that the bean fly is mostly attacked by hymenopterous pupal parasitoids (see Waterhouse 1998). Over 50 species have now been recorded. The most important species are in the family Braconidae and superfamily Chalcidoidea. In general, the recorded parasitism levels have been quite low but exceptions include that from the braconid Opius phaseoli Fischer in East Africa, and this species plus the Eurytomid Eurytoma sp. in India, where in both cases, parasitism levels of 90% or more were observed. Only introduction biological control has been used against the bean fly and an extensive review is provided by Waterhouse (1998). The parasitoids Opius phaseoli and O. importatus Fischer were introduced into Hawaii from Uganda in 1969; and the former species from Hawaii into Taiwan in 1974–75. In Hawaii, the parasitoids did produce acceptable control in most months for several years but their subsequent effectiveness became reduced possibly due to increased use of insecticides. The outcome of the introductions in Taiwan are unknown. Fungal inoculation of bean plants by various endophytes reduces feeding and oviposition by the “bean fly”, a common name encompassing Ophiomyia phaseoli, Ophiomyia spencerella and Ophiomyia centrosematis, thus raising the possibility of fungal endophytes as management tools for these species (Mutune et al. 2016).

“Asparagus Miner”

(Figs 106–115)

Identification & Diagnosis. Like most Ophiomyia, Ophiomyia simplex is small (wing length 2.1–2.5 mm) and entirely black (Figs 106–108) with the anterior margin of the clypeus straight (Fig. 109), but it is otherwise quite distinct. Unlike most congeners, neither the buccal cavity nor the clypeus are narrowed, the facial keel is very shallow and without a medial bulb, the gena is not projecting, and the male vibrissa is not multiplicated to form a “horn”. Also unusual for Ophiomyia is a costa that only extends to vein R₄₊₅, and the orbital plate and parafacial are shining, relatively thick and easily viewed laterally. With regards to the male genitalia, the basiphallus is composed on one pair of narrow twisting bands, and the distiphallus is small and bell-shaped (Figs 111, 112).

Distribution. Ophiomyia simplex is known from north temperate regions and Hawaii in association with cultivated asparagus.

•Australian Region: United States (Hawaii) (Hardy and Delfinado 1980).

•Nearctic Region: Widespread in asparagus growing regions of North America, including California, New York (Spencer and Steyskal 1986), Ontario and Quebec (Spencer 1969).

•Palaearctic Region: Albania, Austria, British Isles, Denmark, France, Germany, Greece, Hungary, Italy, Poland, Turkey (see Papp and Černý (2015), Ukraine (Guglya 2011).

Hosts. Ophiomyia simplex is a stem feeding pest of asparagus (Asparagus officinalis - Asparagaceae).

Damage. This species is of substantial economic concern in the asparagus production industry. Mining by the larvae in the cortex at the base of the stem can cause cosmetic injury and thus affects yield and marketing (Michigan State University Extension 2011). However larval feeding activity may cause more direct damage by cracking and splitting the epidermis, and/or girdling the plant, resulting in yellowing and sometimes plant death. Heavy infestation may result in rot, structurally weakening the plant to the point where wind or rain may break the stem. As a portion of photosynthesis occurs in the green asparagus stem (Downton and Törökfalvy 1975), larval damage reduces productivity.

Ophiomyia simplex has been additionally implicated with “early decline” syndrome in asparagus, wherein Fusarium Link species contribute to crown and root rot, reducing yield to the point where it may not be profitable to harvest (Morrison et al. 2011). The species is suspected of vectoring the fungus, with pathogenic Fusarium found on the larva, pupa, adult, larval mine and frass (Ferro and Gilbertson 1982; Gilbertson et al. 1985; Tuell and Hausbeck 2008). The species has been positively shown to be an exacerbating factor in the rot, with rot damage proportionate to mine number (Damicone et al. 1987). Infected plants, visibly symptomatic by midsummer, are characterized by “wilting, dwarfing, chlorosis, browning of vascular tissue, death to the growing point, and damping off in seedlings”, and current-day crops in Michigan are productive for only half of the time they were in the 1950’s (Morrison et al. 2011).

Biology. In Western Europe and in North America, adults emerge in the late spring; there are two generations per year, with the second overwintering as pupae (Ferro and Gilbertson 1982; Spencer 1973).

After mating, adult females are attracted to young plants in fern. On the plant, they feed at the base of un-opened flowers but oviposit near the base of the stems; this can be either just above or below the soil surface (Ferro and Gilbertson 1982). On hatching, the larvae first tunnel up the stem for up to 30 cm and then reverse, and tunnel downwards, sometimes entering into the tap root. As many as nine larvae have been reported per inch of stem. The mature larvae pupate close to the epidermis and this mostly occurs at or about 3 cm below the soil early in the season, whereas the later overwintering pupae are usually found around 5–7 cm down (Lampert et al. 1984). However, if they mature before they reach this level, they pupate in the root or up the main stem (Barnes 1937); in some cases, pupae have been recovered over 17 cm below ground. The total life cycle (egg to adult) takes between 1500 and 2000 degree-days (Morrison III et al. 2014a).

Movement & Dispersal. The adults are strong fliers and most active above temperatures of 16°C. In asparagus crops in Massachusetts, USA, during hot spells with temperatures in excess of 30°C, the adults disperse to weedy areas around crops (Ferro and Gilbertson 1982).

Management. Early detection. In Massachusetts, USA, yellow sticky stakes have been effective in monitoring adult populations in asparagus crops (Ferro and Suchak 1980). At local levels, a degree-day model that predicts timing of events in the phenology of the miner has been produced; this provides farmers advanced warning of the times to make management interventions to prevent population outbreaks (Morrison III et al. 2014a).

Control. Recommendations in the USA include the clearing of all wild or old stalks of asparagus from fields before the growing season and to use Fusarium-resistant cultivars (University of Massachusetts Extension 2015). Broad spectrum insecticides are mostly used by growers in the USA (Michigan State University Extension 2011). Studies in the UK and the USA have shown that in both regions, the miner is attacked by several species of hymenopterous parasitoids, mostly in the families Braconidae, Eulophidae, and Pteromalidae. In the USA, species of Pteromalidae were the most common (Barnes 1937; Michigan State University Extension 2011; Morrison III et al. 2014b). Conclusions of this research are that efforts should be made to conserve these parasitoids in asparagus fields (Morrison III et al. 2014b).