Preferred name: Liriomyza trifolii
Authority: (Burgess)
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Diptera: Agromyzidae
Other scientific names: Liriomyza alliovora Frick, Liriomyza phaseolunata (Frost)
Common names in English: American serpentine leaf miner, chrysanthemum leaf miner
view more common names online...
Notes on taxonomy and nomenclature EPPO Categorization: A2 list
EU Categorization: PZ Quarantine pest (Annex III)
view more categorizations online...
EPPO Code: LIRITR

Agromyzidae are usually restricted to a limited number of host plants but a few species are highly polyphagous and have become important pests. Liriomyza trifolii is one of these species and causes severe damage to vegetable crops such as celery (Spencer, 1982) and ornamentals such as chrysanthemums (Spencer, 1973).

L. trifolii has been recorded from 29 families.

Host list: Abelmoschus esculentus, Allium cepa, Allium fistulosum, Allium porrum, Allium sativum, Allium schoenoprasum, Apium graveolens, Arachis hypogaea, Argyranthemum frutescens, Artemisia vulgaris, Asteraceae, Baccharis halimifolia, Beta vulgaris, Bidens alba, Bidens pilosa, Brassica juncea, Brassica oleracea var. viridis, Brassica rapa subsp. chinensis, Brassica, Callistephus chinensis, Capsicum annuum, Capsicum chinense, Chenopodium album, Chrysanthemum indicum, Chrysanthemum x morifolium, Chrysanthemum, Cirsium arvense, Citrullus lanatus, Coffea arabica, Coffea canephora, Crotalaria incana, Cucumis melo, Cucumis sativus, Cucumis, Cucurbita pepo, Dahlia hybrids, Daucus carota, Dianthus caryophyllus, Emilia sonchifolia, Erechtites hieraciifolius, Eupatorium caelestinum, Eupatorium serotinum, Flaveria trinervia, Gaillardia aristata, Galinsoga quadriradiata, Gerbera jamesonii, Gossypium barbadense, Gossypium hirsutum, Gypsophila paniculata, Helianthus annuus, Heliotropium europaeum, Helminthotheca echioides, Hymenopappus scabiosaeus, Kallstroemia maxima, Lactuca canadensis, Lactuca sativa, Lactuca serriola, Lathyrus, Leucanthemum vulgare, Leucanthemum x superbum, Luffa aegyptiaca, Medicago lupulina, Medicago sativa, Melanthera nivea, Melilotus albus, Melilotus indicus, Ocimum basilicum, Packera glabella, Pericallis x hybrida, Phaseolus coccineus, Phaseolus lunatus, Phaseolus vulgaris, Picris hieracioides, Pisum sativum, Solanum americanum, Solanum lycopersicum, Solanum melongena, Solanum nigrum, Solanum tuberosum, Sonchus asper, Sonchus oleraceus, Spinacia oleracea, Symphyotrichum novi-belgii, Synedrella nodiflora, Tagetes erecta, Tagetes patula, Tanacetum parthenium, Tanacetum vulgare, Tribulus terrestris, Tridax procumbens, Trifolium repens, Trifolium, Tropaeolum majus, Vicia villosa, Vigna radiata, Vigna unguiculata, Vigna, Zinnia, herbaceous ornamental plants, vegetable plants

L. trifolii originates from North America and spread to other parts of the world in the 1960-1980s. A detailed review of its spread is given in Minkenberg (1988). Today, it is present in South America, Europe, Africa, Asia and Oceania.

EPPO Region: Austria, Belgium, Bosnia and Herzegovina, Croatia, Cyprus, Finland, France (mainland), Greece (mainland, Kriti), Israel, Italy (mainland, Sardegna, Sicilia), Jordan, Malta, Moldova, Morocco, Netherlands, Portugal (mainland), Romania, Russia (Central Russia, Southern Russia), Serbia, Spain (mainland, Islas Canárias), Switzerland, Tunisia, Türkiye
Africa: Benin, Cote d'Ivoire, Egypt, Ethiopia, Guinea, Kenya, Madagascar, Mauritius, Mayotte, Morocco, Nigeria, Reunion, Senegal, South Africa, Sudan, Tanzania, Tunisia, Zambia, Zimbabwe
Asia: China (Anhui, Fujian, Gansu, Guangdong, Guangxi, Guizhou, Hainan, Hebei, Henan, Hubei, Hunan, Jiangsu, Jiangxi, Liaoning, Shaanxi, Shandong, Shanghai, Yunnan, Zhejiang), India (Andhra Pradesh, Delhi, Gujarat, Haryana, Karnataka, Kerala, Madhya Pradesh, Maharashtra, Nagaland, Odisha, Punjab, Tamil Nadu, Telangana, Tripura, Uttar Pradesh, West Bengal), Indonesia, Iran, Israel, Japan (Honshu, Kyushu), Jordan, Korea, Republic, Lebanon, Maldives, Oman, Philippines, Saudi Arabia, Taiwan, United Arab Emirates, Vietnam, Yemen
North America: Canada (Alberta, Nova Scotia, Ontario, Québec), Mexico, United States of America (Arizona, California, Delaware, District of Columbia, Florida, Hawaii, Indiana, Iowa, Maryland, Massachusetts, Michigan, Mississippi, Nevada, New Jersey, New Mexico, New York, North Carolina, Ohio, Pennsylvania, South Carolina, Texas, Virginia, Washington, Wisconsin)
Central America and Caribbean: Bahamas, Barbados, Bermuda, Costa Rica, Cuba, Dominican Republic, Guadeloupe, Guatemala, Martinique, Netherlands Antilles, Puerto Rico, St Kitts-Nevis, Trinidad and Tobago, Virgin Islands (British), Virgin Islands (US)
South America: Argentina, Brazil (Bahia, Espirito Santo, Minas Gerais, Para, Pernambuco, Sao Paulo), Chile, Colombia, Ecuador, French Guiana, Guyana, Peru, Venezuela
Oceania: American Samoa, Australia (Queensland, Western Australia), Fiji, Guam, Micronesia, Northern Mariana Islands, Samoa, Tonga

The principal biological characteristics which make certain Liriomyza spp. particularly successful pests are their rapid population growth and their ability to attack a wide range of different host plants (Reitz et al., 2013).

Details about the life history of Liriomyza trifolii are summarized from Harris & Tate (1933), Lanzoni et al. 2002, Leibee (1982), Minkeberg (1988), Parrella et al. (1981), Parrella (1987), Spencer (1973), Tokumaru & Abe (2003, 2005).

Copulation takes place on the day when females emerge. Non-fertilized females are not able to oviposit. After mating female flies puncture the leaf surface of the host plants with their ovipositor causing wounds which serve as sites for feeding or oviposition. Males can also take advantage of these feeding sites as they are less well equipped for puncturing plant tissue. Feeding punctures can be used for egg laying with approximately 15% of punctures containing eggs.

Eggs are inserted just below the leaf surface. L. trifolii females lay on average 11.5 eggs per day. The number of eggs laid depends on the host plant. The duration of the egg stage varies from 1 to 7 days depending on the temperature and host plant. Female flies live longer than males.

There are three larval instars which, in total, last 4 to 7 days at mean temperatures above 24°C. Larval feeding forms irregular linear mines. Just before pupation, mature larvae cut semi-circular exit slits in the upper surface of the leaves. After a short period, larvae drop to the ground and burrow just below the surface of the soil or in crop debris before pupating. The pupal stage lasts from 7 to 33 days depending on temperature.

In the Southern USA, the life-cycle is probably continuous throughout the year. There is a noticeable first generation which reaches a peak in April (Spencer, 1973). In Southern Florida, L. trifolii has two or three complete generations followed by a number of incomplete, overlapping generations (Spencer, 1973).

Symptoms

The most important damage caused by Liriomyza spp. is due to larval mining in the leaf tissue. Larval mining reduces the aesthetic value of ornamentals, decreases the photosynthetic capacity of leaves and can ultimately cause defoliation in severe cases (Spencer, 1973). Mines are irregular linear structures in the leaf tissue. They are off-white with trails of dark frass in their margins.

Liriomyza spp. adults cause two main types of damage to their host plants, feeding and oviposition punctures (Reitz et al., 2013; Minkeberg & van Lenteren, 1986). Adult feeding and oviposition punctures reduce the aesthetic value of ornamental plants and can lead to death of young plants by reducing photosynthetic capacity. Punctures can also be invaded by fungi and bacteria causing additional damage to host plants. Feeding punctures appear as uneven rounded white speckles on the leaf surface whereas oviposition punctures are smaller and more rounded. These symptoms are not used as a diagnostic character as there is no variation between Liriomyza spp.

Morphology

Detailed description of the morphology of immature and adult L. trifolii is given in Spencer (1973). The main diagnostic characters of the four regulated Liriomyza spp. (L. bryoniae, L. huidobrensis, L. sativae and L. trifolii) can be found in the IPPC diagnostic protocol for the genus Liriomyza (IPPC, 2017) and the EPPO Standard on diagnostics PM 7/53 (2) Liriomyza spp. (EPPO, 2022a) The following sections summarize this information.

Eggs

Oval and white, 0.25 mm long.

Larva

There are three larval stages that range from 0.5 mm in length for the first instar to 3.0 mm for the last one. Their shape is cylindrical and tapering towards the head. The posterior spiracles are tricorn-shaped with three pores located on projections. Newly emerged L. trifolii larvae are translucent and turn yellow-orange in the later stages.

Puparium

Oval cylinder in shape of about 2.0 mm, yellowish brown. The spiracles are still visible in the pupal stage.

Adult

Small 1-3 mm long mostly black flies, with a yellow frons and scutellum. The orbital setulae are reclinate, the costa extends to vein M₁₊₂ and the femora are predominantly yellow. Male genitalia are characteristic of the genus.

Detection and inspection methods

There are more than 400 species of Liriomyza (GBIF, 2023) and their morphological identification relies on the male genitalia. Adult females can only be used for genus level identification. Likewise, there are no keys available for species level identification of the immature stages. L. trifolii males can thus be separated from the very similar L. bryoniae, L. huidobrensis, L. sativae and L. strigata by the structure of their distiphallus (terminal part of the intromittent organ) which has one distal bulb with a marked constriction between its apical and basal parts. The basal section of the bulb is strongly curved (IPPC, 2017; EPPO, 2022a).

The mines caused by larval feeding can also be useful for detection but this character should be used in combination with other characters as mine pattern is influenced by environmental factors (EPPO, 2022a). Other flies as well as some Lepidoptera are known to have leaf-mining larvae and can potentially be confused with Agromyzidae. Nonetheless, the characteristic feeding punctures of Liriomyza spp. allows diagnosticians to differentiate them from other leafminers.

In the absence of male adults for morphological identification, the following molecular tests can be used for L. trifolii species identification: PCR RFLP targeting the COII gene (Kox et al., 2005), conventional multiplex PCR targeting the COI gene (Nakamura et al., 2013), an on-site LAMP test, multiplex real-time PCR (Sooda et al., 2017), and DNA barcoding based on the COI gene (EPPO, 2021). These molecular techniques are summarized in the EPPO and the IPPC diagnostic protocols for regulated Liriomyza species (EPPO, 2022a; IPPC, 2017). Recently, molecular identification based on next generation sequencing techniques are also being developed (Frey et al., 2022).

Adults are capable of limited flight and can be dispersed by wind currents (see Malipatil et al., 2016 for references), but are unlikely to spread over long distances. The high degree of polyphagy of L. trifolii as well as the concealed lifestyle of its larvae make its dissemination through the movement of plant material the most likely mean of colonizing new countries (EFSA, 2012; Parrela, 1987, Reitz et al., 2013). L. trifolii is regularly intercepted in trade, in particular on leafy vegetables and cut flowers (Europhyt, 2023).

Economic impact

Liriomyza spp. are highly polyphagous and invasive and cause severe damage to vegetable crops and ornamentals through adult feeding, oviposition and larval mining. L. trifolii originates from North America but is now present worldwide (CABI, 2021).

This species is a major pest of chrysanthemums (Spencer, 1973) and celery (Spencer, 1982) in the USA and near total production loss of chrysanthemums has been reported in California (Newman & Parrella, 1981).

Control

The most common control strategy for Liriomyza spp. is the extensive use of chemical control methods. However, Liriomyza spp. are known to readily develop insecticide resistance (Reitz et al., 2013), unlike their local parasitoids, thus causing serious leafminer outbreaks. Some insecticides are effective against Liriomyza spp. (Schuster & Everett, 1983). These are translaminar and target the larvae inside the leafmines. Biological control methods are increasingly used in horticultural industries and commercial vegetable production (Liu et al. 2009). There are more than 140 described species of Liriomyza parasitoids and these are the primary agents used in biological control strategies. In open fields, integrated pest management strategies promoting local parasitoid diversity are commonly used to control Liriomyza spp. In the more controlled greenhouse environments, commercially available parasitoids, such as species in the genus Diglyphus, are also reported to successfully regulate Liriomyza infestations. Predators and entomopathogenic nematodes and fungi are also known but there are a limited number of species and they are not considered as efficient control agents.

Phytosanitary risk

Liriomyza trifolii is a highly polyphagous species present in Europe essentially in the Mediterranean region. The main dispersal mechanisms is through the trade related movement of plant material hosting the immature stages of L. trifolii (EFSA, 2012). The latter are cryptic and can easily go undetected in plants for planting, soil, fruit and vegetables, cut flowers and branches with foliage.

It can be recommended that host plants for planting from countries where L. trifolii is present are inspected over three months at regular intervals before export can take place, to verify the absence the pest itself or any signs of its presence. General guidance on how to conduct inspections of places producing vegetable plants for planting under protected conditions can be found in the EPPO Standard PM 3/77 (EPPO, 2022b). In the European Union, specific measures are taken to protect areas that are still free from L. trifolii (Protected Zones), which means that plant material should respect a list of established rules (Commission implementing regulation (EU) 2021/2285) before being cleared for import into the Protected Zones.

CABI (2021) Datasheet on Liriomyza trifolii. https://www.cabidigitallibrary.org/doi/full/10.1079/cabicompendium.30965

EFSA Panel on Plant Health: Baker R, Bragard C, Candresse T, Gilioli G, Grégoire J-C, Holb I, Jeger MJ, Evtimova Karadjova O, Magnusson C, Makowski D, Manceau C, Navajas M, Rafoss T, Rossi V, Schans J, Schrader G, Urek G, van Lenteren JC, Vloutoglou I, Winter S and van der Werf W (2012) Scientific opinion on the risks to plant health posed by Liriomyza huidobrensis (Blanchard) and Liriomyza trifolii (Burgess) in the EU territory, with the identification and evaluation of risk reduction options. EFSA Journal 10(12), 3028. https://doi.org/10.2903/j.efsa.2012.3028

EPPO (2021) EPPO Standards. Diagnostics. PM 7/129 (2) DNA barcoding as an identification tool for a number of regulated pests: DNA barcoding Arthropods. EPPO Bulletin 51(1), 100–143.

EPPO (2022a) EPPO Standards. Diagnostics. PM 7/53 (2) Liriomyza spp. EPPO Bulletin 52, 326-345.

EPPO (2022b) EPPO Standards. Phytosanitary Procedures. PM 3/77 (2) Vegetable plants for planting under protected conditions - Inspection of places of production. EPPO Bulletin 52(3), 526-543.

Europhyt (2023) Interceptions of harmful organisms in imported plants and other objects. European Commission. https://food.ec.europa.eu/plants/plant-health-and-biosecurity/europhyt/interceptions_en [last accessed 2023-10].

Frey JE, Frey B, Frei D, Blaser S, Gueuning M & Bühlmann A (2022) Next generation biosecurity: Towards genome based identification to prevent spread of agronomic pests and pathogens using nanopore sequencing. PloS one 17(7), e0270897. https://doi.org/10.1371/journal.pone.0270897

GBIF. Liriomyza Mik, 1894 in GBIF Secretariat. GBIF Backbone Taxonomy. Checklist dataset. https://doi.org/10.15468/39omei [accessed via GBIF.org on 2023-10-01].

Harris HM & Tate HD (1933) A leafminer attacking the cultivated onion. Journal of Economic Entomology 26, 515-516.

IPPC (2017) DP 16: Genus Liriomyza. International Standard for Phytosanitary measures 27, annex 16. https://www.ippc.int/static/media/files/publication/en/2017/01/DP_16_2016_En_2017-01-30.pdf

Kox LFF, Van Den Beld H E, Lindhout B I & De Goffau LJW (2005) Identification of economically important Liriomyza species by PCR‐RFLP analysis. EPPO Bulletin 35(1), 79-85.

Lanzoni A, Bazzocchi GG, Burgio G & Fiacconi MR (2002) Comparative life history of Liriomyza trifolii and Liriomyza huidobrensis (Diptera: Agromyzidae) on beans: effect of temperature on development. Environmental Entomology 31(5), 797-803.

Leibee GL (1982) Development of Liriomyza trifolii on celery. In: Proceedings of IFAS-Industry Conference on Biology and Control of Liriomyza leafminers, Lake Buéna Vista, Florida (Ed. by Schuster DJ), pp. 35-41.

Liu T-X, Kang Le, Heinz KM and Trumble J (2009) Biological control of Liriomyza leafminers: progress and perspective. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 4, 004.

Malipatil M, Blacket M, Wainer J, Ridland P & Reviewer Jones DC (Subcommittee on Plant Health Diagnostics) (2016) National Diagnostic Protocol for Liriomyza trifolii – NDP27 V1. https://www.plantbiosecuritydiagnostics.net.au/app/uploads/2018/11/NDP-27-American-serpentine-leaf-miner-Liriomyza-trifolii-V1.pdf

Minkenberg OPJM & van Lenteren JC (1986) The leafminers Liriomyza bryoniae and L. trifolii (Diptera: Agromyzidae), their parasites and host plants: a review. Agricultural University Wageningen Papers No. 86-2, 50 pp.

Minkenberg OPJM (1988) Dispersal of Liriomyza trifolii. EPPO Bulletin 18, 173-182.

Nakamura S, Masuda T, Mochizuki A, Konishi K, Tokumaru S, Ueno K & Yamaguchi T (2013) Primer design for identifying economically important Liriomyza species (Diptera: Agromyzidae) by multiplex PCR. Molecular Ecology Resources 13, 96–102.

Newman JP & Parrella MP (1986) A license to kill. Greenhouse Manager 5(3), 86-92.

Parrella MP, Allen WW & Marishita P (1981) Leafminer species causes California chrysanthemum growers new problems. California Agriculture 35, 28-30.

Parrella MP (1987) Biology of Liriomyza. Annual Review of Entomology 32(1), 201-224.

Reitz SR, Gao Y & Lei Z (2013) Insecticide use and the ecology of invasive Liriomyza leafminer management. Insecticides-development of safer and more effective technologies. In: Insecticides. Development of safer and more effective technologies (ed. Trdan S) IntechOpen, 235-255. http://dx.doi.org/10.5772/53874

Sakamaki Y, Miura K & Chi Y (2005) Interspecific hybridization between Liriomyza trifolii and Liriomyza sativae. Annals of the Entomological Society of America 98(4), 470-474.

Scheffer SJ & Lewis ML (2006) Mitochondrial phylogeography of the vegetable pest Liriomyza trifolii (Diptera: Agromyzidae): Diverged clades and invasive populations. Annals of the Entomological Society of America 99(6), 991–998.

Schuster DJ & Everett PH (1983) Response of Liriomyza trifolii (Diptera: Agromyzidae) to insecticides on tomato. Journal of Economic Entomology 76(5), 1170-1174.

Sooda A, Gunawardana D, Li D & Kumarasinghe L (2017) Multiplex real‐time PCR assay for the detection of three invasive leafminer species: Liriomyza huidobrensis, L. sativae and L. trifolii (Diptera: Agromyzidae). Austral Entomology 56(2), 153-159.

Spencer KA (1973) Agromyzidae (Diptera) of economic importance. Series Entomologica 9, 418 pp. Junk, The Hague, Netherlands.

Spencer KA (1982) US celery under threat. Grower 97, 15-18.

Tokumaru S & Abe Y (2003) Effects of temperature and photoperiod on development and reproductive potential of Liriomyza sativae, L. trifolii, and L. bryoniae (Diptera: Agromyzidae). Japanese Journal of Applied Entomology and Zoology 47(4), 143-152.

Tokumaru S & Abe Y (2005) Effects of host plants on the development and host preference of Liriomyza sativae, L. trifolii, and L. bryoniae (Diptera: Agromyzidae). Japanese Journal of Applied Entomology and Zoology 49(3), 135-142.

This datasheet was extensively revised in 2024 by Sarah Chérasse, ANSES. Her valuable contribution is gratefully acknowledged.

EPPO (2024) Liriomyza trifolii. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-11-24)

This datasheet was first published in the EPPO Bulletin in 1984 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2024. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1^st and 2^nd edition). CABI, Wallingford (GB).

EPPO (1984) Data sheets on quarantine organisms No. 131 Liriomyza trifolii. EPPO Bulletin 14(1), 29-37. https://doi.org/10.1111/j.1365-2338.1984.tb01978.x