Pea leaf miner Liriomyza huidobrensis Blanchard Diptera: Agromyzidae

Islamic Republic Of Iran Ministry of Jihad-e-Agriculture Plant Protection Organization A Guide for Diagnosis & Detection Of Quarantine Pests Pea leaf miner Liriomyza huidobrensis Blanchard Diptera: Agromyzidae Edited by: Ahmad Cheraghian Bureau of Plant Pest Surveillance and Pest Risk Analysis 2014

Liriomyza huidobrensis (Blanchard, 1926) Diptera: Agromyzidae Common name: Pea leaf miner, serpentine leaf miner, South American leaf miner Synonyms: Liriomyza cucumifoliae Blanchard, 1938, Agromyza huidobrensis Blanchard, 1926 Liriomyza dianthi Frick, 1958, Liriomyza langei Frick, 1951 Liriomyza decora Blanchard, 1954 Economic impact: L. huidobrensis is a serious pest of potato, vegetables and ornamental plants in the field and glasshouses in many parts of the world (Lange et al., 1957). In South America, it is a key pest of potato. In Europe and Mediterranean regions, L. huidobrensis is already a major pest of chrysanthemums, Primula spp., Verbena, lettuces (OEPP/EPPO, 1994), Phaseolus vulgaris, cucumbers, celery and Cucurbita pepo (ADAS, 1991). Treatments for chrysanthemums are recommended if 50 larvae are found in a random sample of the upper two-thirds of 10 stems (Spencer, 1982). Since it has spread to Mediterranean countries, it has appeared on outdoor crops, such as lettuce and sugarbeet (Echevarria et al., 1994). Although it initially proved to be a much more serious pest than L. trifolii in Israel (Weintraub and Horowitz, 1995), it has since come under natural biological control and is only occasionally a pest. Damage is caused by larvae mining into leaves and petioles. The photosynthetic ability of the plants is often greatly reduced as the chlorophyll-containing cells are destroyed (Parrella and Bethke, 1984). Severely infested leaves may fall, exposing plant stems to wind action, and flower buds and developing fruit to scald (Musgrave et al., 1975). The presence of unsightly larval mines and adult punctures in the leaf palisade of ornamental plants can further reduce crop value (Smith et al., 1962; Musgrave et al., 1975). In young plants and seedlings, mining may cause considerable delay in plant development, leading to plant loss. Hosts: Major hosts: Allium cepa (onion), Allium sativum (garlic), Apium graveolens (celery), Chrysanthemum morifolium (chrysanthemum (florists')), Cucurbita pepo (ornamental gourd), Galinsoga, Gypsophila paniculata (babysbreath), Lactuca sativa (lettuce), Phaseolus vulgaris (common bean), Pisum sativum var. arvense (Austrian winter pea). Minor hosts: Amaranthus (grain amaranth), Amaranthus retroflexus (redroot pigweed), Aster, Beta vulgaris (beetroot), Calendula (marigolds), Capsicum annuum (bell pepper), Chenopodium quinoa (quinoa), Cucumis melo (melon), Cucumis sativus (cucumber), Datura (thorn-apple), Gerbera (Barbeton daisy), Lathyrus (Vetchling), Linum (flax), Lycopersicon esculentum (tomato), Medicago sativa (lucerne), Melilotus (melilots), Petunia, Solanum melongena (aubergine), Solanum tuberosum (potato), Spinacia oleracea (spinach), Tagetes (marigold), Tropaeolum, Valerianella locusta (common cornsalad), Verbena (vervain), Vicia faba (broad bean), Zinnia elegans (zinnia). Wild hosts:bidens pilosa (blackjack), Emilia sonchifolia (red tasselflower), Galinsoga parviflora (gallant soldier), Oxalis (wood sorrels), Portulaca oleracea (purslane), Sonchus (Sowthistle).

Geographic distribution: Asia:China, India, Indonesia, Israel, Jordan, Korea, DPR, Lebanon, Malaysia, Philippine, Singapore, Sri Lanka, Syria, Thailand, Turkey, Vietnam. Europe: Austria, Belgium, Bulgaria, Corsica, Cyprus,Czechoslovakia, Finland, France, Germany, Greece, Hungary, Italy, Malta, Netherlands, Norway, Poland, Portugal, Spain, Switzerland, United Kingdom. Africa:Comoros, Mauritius, Réunion, Seychelles, South Africa. North America: Canada, U.S.A., Central America: Belize, Costa Rica, Dominican Republic, El Salvador, Guadeloupe, Guatemala, Honduras, Nicaragua, Panama. South America:Argentina, Brazil, Chile, Colombia, Ecuador, French Guiana, Peru, Uruguay, Venezuela. Australia and Pacific Island: Guam. World distribution map of Liriomyza huidobrensis Morphology: Eggs: Size 0.2-0.3 mm x 0.10-0.15 mm, off-white and slightly translucent. Eggs of Liriomyza huidobrensis

Larva: A maggot up to 3.25 mm in length. First-instar larvae are colourless on hatching, turning pale yellow-orange. Later instars are yellow-orange. The ratio of the cephalopharyngeal skeletons between the first and second instars is 1.80 and between the second and third instars is 1.47 (Head et al., 2002). The posterior spiracle forms a crescent with six to nine mounted pores. Larva of Liriomyza huidobrensis Pupae: The puparium is oval, slightly flattened ventrally, 1.3-2.3 0.5-0.75 mm, with variable colour from light brown to almost black. Pupae of Liriomyza huidobrensis Adult: Small, greyish-black, compact-bodied, 1.3-2.3 mm in body length, 1.3-2.3 mm in wing length. Females are slightly larger than males. In general, any agromyzid of this size with a bright yellow central area of the scutellum and bright yellow areas of the head and pleura, belongs to the genus Liriomyza. The subfamily Phytomyzinae has vein Sc becoming a fold distally, but not coalescing with vein R1 before reaching C; the genus Liriomyza has orbital setulae which are not proclinate (they may be reclinate or absent); 2 pairs orbital setae; C extending to M, which end in wing apex; cross vein DM-Cu present; scutellum yellow. L. huidobrensis may be distinguished from other Liriomyza species by the head and leg yellow parts being a darker orange-yellow, the third antennal segments very dark, sometimes almost black on top, and the mesoplura is largely black. The overall appearance is of a small dark fly. Adult of Liriomyza huidobrensis

Abdomen segment lateral view dorsal view prothorax dorsal view prothorax lateral view scutellum yellow head and front with setae head fore wing apex; cross vein DM-Cu present Femur and tibia male genitalia Adult of Liriomyza huidobrensis

Eggs of Liriomyza huidobrensis Larva of Liriomyza huidobrensis Pupae of Liriomyza huidobrensis Adult of Liriomyza huidobrensis

Biology and ecology: Peak emergence of adults occurs before midday (McGregor, 1914). Males usually emerge before females. Mating takes place from 24 h after emergence and a single mating is sufficient to fertilize all eggs laid. Female flies puncture the leaves of the host plants causing wounds which serve as sites for feeding or oviposition (Mujica and Cisneros, 1997). Feeding punctures cause the destruction of a larger number of cells and are more clearly visible to the naked eye. Approximately 15% of punctures made by L. trifolii and L. sativae contain viable eggs (Parrella et al., 1981). Males are unable to puncture leaves, but have been observed feeding at punctures produced by females. Both males and females are able to survive on dilute honey (in the laboratory) and take nectar from flowers. Eggs are inserted just below the leaf surface. The number of eggs laid varies according to temperature and host plant. Eggs hatch in 2-5 days according to the temperature. The duration of larval development is generally 4-7 days at mean temperatures above 24 C (Harris and Tate, 1933). Reductions in population levels of L. huidobrensis occurred in California, USA, when the daily maximum temperature rose to 40 C (Lange et al., 1957). There are three larval stages that feed within the leaves. The larvae predominantly feed on the plant in which the eggs are laid. Although the larvae of some species can exit one leaf and enter another, this has not been reported for L. huidobrensis. The larva leaves the plant to pupate (Parrella and Bethke, 1984). Pupae may be found in crop debris or in the soil. Pupation takes place within the sclerotized skin of the third larva and gives rise to adult flies. Parthenogenic females have not been reported. Pupariation is adversely affected by high humidity and drought. Adult emergence occurs 7-14 days after pupariation, at temperatures between 20 and 30 C (Leibee, 1982). At low temperatures emergence is delayed. In southern USA, the life cycle is probably continuous throughout the year, although there is a noticeable first generation which reaches a peak in April (Spencer, 1973). In Israel, adults can be found from the autumn to late spring but not in summer (Weintraub and Horowitz, 1996). Adults are primarily active in early morning, shortly after sunrise, and again just before sunset (Weintraub and Horowitz, 1996). In California, USA, it completes its life cycle in 17-30 days during the summer and in 50-65 days during the winter (Lange et al., 1957). Adults generally live for 15-30 days, and females generally live longer than males. In northern Europe, L. huidobrensis is mainly a glasshouse pest, but a proportion of puparia can survive outdoors during an average Dutch winter (van der Linden, 1993). In Peru, the life cycle is as follows: egg stage (3-4 days); first-instar larva (3-4 days); second-instar larva, 2-3 days; third instar 3-4 days; pupal stage (12-18 days). Females had an average longevity of 3-28 days; male longevity was 2-6 days. The mean number of eggs laid per female in winter was 117 and in spring was 161 (Mujica and Cisneros, 1997). Studies on L. huidobrensis developmental rates in lettuce at different constant temperatures (11 to 28±1 C) revealed a linear increase with temperature (Head et al., 2002). The theoretical lower threshold temperatures for development for each larval instar and pupae were 5.35, 6.30, 6.20 and 5.7 C, respectively. The calculated degreedays for each stage were 84.3, 30.1, 58.9 and 143.7, respectively. Similar studies were performed on beans (15-30 C )(Lanzoni et al., 2002). They estimated the minimum developmental temperatures for egg, larva and pupa at 8.1, 7.7 and 7.3 C, respectively. The upper thresholds for egg, larva and pupa were calculated to be 31.1, 35.3, and 27.9 C, respectively. Their data are similar to Prando and da Cruz (1986) and Vercambre and De Crozals (1993).

L. huidobrensis is from a tropical to warm temperate region and has been found up to 3000 m and has been shown to be more cold-hardy than its near relative L. sativae (Wang et al., 2000), surviving a super cooling point of -19.55 C and a freezing point of -18.7 C compared to L. sativae with a super cooling point of -9.96 C and a freezing point of -9.06 C. This behaviour gives L. huidobrensis a far greater climatic range for survival. Indeed, Chen and Kang (2004) evaluated populations in China from 25 N to 42 N and found increasing cold tolerance with latitude. Supercooling capacity ranged down to -23.9 C. Even in severe cold, some leafminers were able to survive. Interestingly, Martin et al. (2005) found that no L. huidobrensis survived the winter in southern Ontario, Canada. Life cycle of Liriomyza huidobrensis

Symptoms: Feeding punctures appear as white speckles between 0.13 and 0.15 mm in diameter. Oviposition punctures are smaller (0.05 mm) and are more uniformly round. The larva is primarily a leaf miner (on peas the larva may also feed on the outer surface of young pods); mines are usually white with dampened black and dried brown areas, and are usually associated with the midrib and lateral leaf veins. Mines are typically serpentine, of irregular shape, increasing in width as larvae mature; there should be no confusion with the mines of the European chrysanthemum leaf miner Chromatomyia syngenesiae which are less contorted and uniformly white. Several larvae feeding on a single leaf may produce a secondary 'blotch' mine type and leaf wilt may occur (Spencer, 1973). In potato, feeding punctures can often be seen all over the growing plant, giving the impression that a generalized outbreak of larval infestation is in process. But the development of the larval damage follows a rather fixed pattern, somewhat different from that of the adult fly population. First, the initial larval infestation and corresponding damage occur in the lower third of the plant, moving upwards to the top of the plant. At this time, practically the whole above ground part of the plant becomes necrotic and dies. Larval damage is consistently less severe during vegetative growth stages than when the plant is full grown. The occurrence of egg extrusion in the growing leaves might explain this phenomenon (Mujica and Cisneros, 1997). Symptoms by affected plant part Fruits/pods: Leaves: internal feeding, Stems: Larval damage of Liriomyza huidobrensis

Larval damage of Liriomyza huidobrensis

Means of moement and dispersal: There is no information on the natural dispersal of L. huidobrensis, and very little information on dispersal in other species. Jones and Parrella (1986) measured the dispersal of L. trifolii in a chrysanthemum greenhouse and found that females flew signigicantly farther than males. Ozawa et al. (1999) measured the height at which L. trifolii fly in a greenhouse and found that they were primarily close to the plants. L. huidobrensis is a larger and stronger fly than L. trifolii. L. huidobrensis is not carried phoretically by any other organism. It can be windblown into crops from surrounding vegetation/fields. Vector transmission Liriomyza spp. do not transmit any pathogens. However, they may enhance the occurrence of plant pathogens. Adult females puncture both the upper and lower leaf surfaces (up to 100 punctures daily) to feed and lay eggs, leaving wounds which can serve as portals for bacteria and fungus and reduce photosynthesis. Since Chandler (1991) showed that the occurrence of leaf punctures from L. trifolii significantly increased the incidence of Alternaria leaf blight lesions (Alternaria cucumerina) on muskmelon leaves (Cucumis melo), it is possible that other leaf pathogens may be enhanced. Phytosanitary significance: L. huidobrensis is a major quarantine pest and is officially listed as such in many areas, for example, EPPO (OEPP/EPPO, 1984). It is primarily a tropical and warm temperate species and has been found up to 3000 m (Spencer, 1973), but in some parts of Europe it has shown an ability to become a major pest of a wide variety of ornamental or vegetable crops grown under glass. The action protocols for the UK (Cheek et al., 1993) provide an example of the contingency plans that should be in place in countries not yet invaded by this pest. And L. huidobrensis is quarantine pest for Iran and some of other Countries. Detection and inspection: Populations of adults may be monitored by placing yellow sticky traps at plant height (Weintraub and Horowitz, 1996), and Heinz and Chaney (1995) discussed action thresholds. Dankowska et al. (2000) used sticky yellow traps enhanced with 3-phenylopropionaldehyde to improve the catch of L. huidobrensis by 60%.. Use of Yellow trap for Detection Liriomyza huidobrensis

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