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Datasheet

Liriomyza trifolii
(American serpentine leafminer)

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Datasheet

Liriomyza trifolii (American serpentine leafminer)

Summary

  • Last modified
  • 22 November 2019
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Natural Enemy
  • Host Animal
  • Preferred Scientific Name
  • Liriomyza trifolii
  • Preferred Common Name
  • American serpentine leafminer
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Uniramia
  •         Class: Insecta
  • Summary of Invasiveness
  • L. trifolii is a leaf-mining insect, commonly known as the serpentine leafminer. It is highly polyphagous and has been recorde...

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Pictures

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PictureTitleCaptionCopyright
Male and female L. trifolii are generally similar in appearance.
TitleAdult male
CaptionMale and female L. trifolii are generally similar in appearance.
Copyright©K.A. Spencer
Male and female L. trifolii are generally similar in appearance.
Adult maleMale and female L. trifolii are generally similar in appearance. ©K.A. Spencer
L. trifolii is very small: 1-1.3 mm body length, up to 1.7 mm in female with wings 1.3-1.7 mm.The scutellum is bright yellow; face, frons and third antennal segment bright yellow.
TitleAdult female
CaptionL. trifolii is very small: 1-1.3 mm body length, up to 1.7 mm in female with wings 1.3-1.7 mm.The scutellum is bright yellow; face, frons and third antennal segment bright yellow.
Copyright©K.A. Spencer
L. trifolii is very small: 1-1.3 mm body length, up to 1.7 mm in female with wings 1.3-1.7 mm.The scutellum is bright yellow; face, frons and third antennal segment bright yellow.
Adult femaleL. trifolii is very small: 1-1.3 mm body length, up to 1.7 mm in female with wings 1.3-1.7 mm.The scutellum is bright yellow; face, frons and third antennal segment bright yellow.©K.A. Spencer
Dorso-lateral view of adult L. trifolii (museum set specimen).
TitleAdult
CaptionDorso-lateral view of adult L. trifolii (museum set specimen).
Copyright©Georg Goergen/IITA Insect Museum, Cotonou, Benin
Dorso-lateral view of adult L. trifolii (museum set specimen).
AdultDorso-lateral view of adult L. trifolii (museum set specimen).©Georg Goergen/IITA Insect Museum, Cotonou, Benin

Identity

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Preferred Scientific Name

  • Liriomyza trifolii Burgess in Comstock, 1880

Preferred Common Name

  • American serpentine leafminer

Other Scientific Names

  • Agromyza phaseolunata Frost, 1943
  • Liriomyza alliivora Frick, 1955
  • Liriomyza alliovora Frick, 1955
  • Liriomyza phaseolunata (Frost, 1943)
  • Oscinis trifolii Burgess in Comstock, 1880

International Common Names

  • English: chrysanthemum leaf miner; serpentine leaf miner
  • Spanish: minador pequeño del frijol
  • French: mineuse du gerbera

Local Common Names

  • Germany: Floridaminierfliege
  • Russian Federation: American clover miner

EPPO code

  • LIRITR (Liriomyza trifolii)

Summary of Invasiveness

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L. trifolii is a leaf-mining insect, commonly known as the serpentine leafminer. It is highly polyphagous and has been recorded from 25 families. As a major pest of ornamental and vegetable crops, including beans (phaseolus), Capsicum, carnations, celery, chrysanthemums (Dendranthenum, the commercial 'Mum'), clover, Cucumis, Gerbera, Gypsophila, lettuces, lucerne, potatoes, Senecio hybridus and tomatoes it has had important biological and economic impacts across a number of countries, including North America, Africa and Europe.<_u13a_p />

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Arthropoda
  •             Subphylum: Uniramia
  •                 Class: Insecta
  •                     Order: Diptera
  •                         Family: Agromyzidae
  •                             Genus: Liriomyza
  •                                 Species: Liriomyza trifolii

Notes on Taxonomy and Nomenclature

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Liriomyza trifolii is one of the truly polyphagous agromyzids and has been recorded in 25 families (Spencer, 1990). It was first described as Oscinis trifolii (Burgess in Comstock, 1880) in the family Chloropidae from flies attacking the leaves of Trifolium repens (white clover) in Indiana, USA. Later, it was transferred to the family Agromyzidae in the genus Agromyza by Coquillet (1898), then to Liriomyza by de Meijere (1925). Spencer, 1973 synonymized Liriomyza alliovora Frick, 1955, breeding in Allium (onions) in Iowa, USA, and in Spencer, 1986, Agromyza phaseolunata Frost (1943, as Liriomyza) attacking Phaseolus lunatus (lima beans) in New Jersey, USA with L. trifolii.
 

Description

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Descriptions of L. trifolii refer to fresh materials. Dry specimens may be distorted due to the manner in which they have been preserved. Also, the age of the specimen, when killed, will have some effect on its preservation characteristics.

For accurate identification, examination of the leaf mine and all stages of development are crucial.

Egg

L. trifolii eggs are 0.2-0.3 mm x 0.1-0.15 mm, off white and slightly translucent.

Larva

This is a legless maggot with no separate head capsule, transparent when newly hatched but colouring up to a yellow-orange in later instars and is up to 3 mm long. L. trifolii larvae and puparia have a pair of posterior spiracles terminating in three cone-like appendages. Spencer (1973) describes distinguishing features of the larvae. Petitt (1990) describes a method of identifying the different instars of the larvae of L. sativae, which can be adapted for use with the other Liriomyza species, including L. trifolii.

Puparium

This is oval and slightly flattened ventrally, 1.3-2.3 x 0.5-0.75 mm with variable colour, pale yellow-orange, darkening to golden-brown. The puparium has posterior spiracles on a pronounced conical projection, each with three distinct bulbs, two of which are elongate. Pupariation occurs outside the leaf, in the soil beneath the plant.

Menken and Ulenberg (1986) describe a method of distinguishing L. trifolii from L. bryoniae, L. huidobrensis, and L. sativae using allozyme variation patterns as revealed by gel electrophoresis.

Adult

L. trifolii is very small: 1-1.3 mm body length, up to 1.7 mm in female with wings 1.3-1.7 mm. The mesonotum is grey-black with a yellow blotch at the hind-corners. The scutellum is bright yellow; the face, frons and third antennal segment are bright yellow. Male and female L. trifolii are generally similar in appearance.

L. trifolii are not very active fliers, and in crops showing active mining, the flies may be seen walking rapidly over the leaves with only short jerky flights to adjacent leaves.

Head
The frons, which projects very slightly above the eye, is just less than 1.5 times the width of the eye (viewed from above). There are two equal ors and two ori (the lower one weaker). Orbital setulae are sparse and reclinate. The jowls are deep (almost 0.33 times the height of the eye at the rear); the cheeks form a distinct ring below the eye. The third antennal segment is small, round and noticeably pubescent, but not excessively so (vte and vti are both on a yellow ground).

Mesonotum
Acrostical bristles occur irregularly in 3-4 rows at the front, reducing to two rows behind. There is a conspicuous yellow patch at each hind-corner. The pleura are yellow; the meso- and sterno-pleura have variable black markings.

Wing
Length 1.3 -1.7 mm, discal cell small. The last section is M<(sub)3+4> from 3-4 times the length of the penultimate one.

Genitalia
The shape of the distiphallus is fairly distinctive but could be mis-identified for L. sativae. Identification using the male genitalia should only be undertaken by specialists.

Colour
The head (including the antenna and face) is bright yellow. The hind margin of the eye is largely yellow, vte and vti always on yellow ground.

The mesopleura is predominantly yellow, with a variable dark area, from a slim grey bar along the base to extensive darkening reaching higher up the front margin than the back margin. The sternopleura is largely filled by a black triangle, but always with bright yellow above.

The femora and coxa are bright yellow, with the tibia and tarsi darker; brownish-yellow on the fore-legs, brownish-black on the hind legs. The abdomen is largely black but the tergites are variably yellow, particularly at the sides. The squamae are yellowish, with a dark margin and fringe.

Although individual specimens may vary considerably in colour, the basic pattern is consistent.

Distribution

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L. trifolii has not yet been reported from many countries where it is actually present. It is generally recognized that all the countries bordering the Mediterranean have L. trifolii in varying degrees and that it occurs in all mainland states of the USA. L. trifolii has been recorded from the Juan Fernandez Islands (an offshore territory of Chile; Martinez and Etienne, 2002; EPPO, 2009). See also CABI/EPPO (1998, No. 96). L. trifolii is apparently unable to overwinter in the open in the north European EPPO countries. However,  the current regulations to prevent entry and spread in non-Mediterranean areas were found to be only partially effective, as interceptions are still being reported (EFSA, 2012).

The record for Argentina has been changed to 'Absent, unreliable record' as Martinez and Etienne (2002) and EPPO (2006) are based on Burgess (in Comstock, 1880 (1879)) and there have been no other reports of the pest in Argentina. L. trifolii is a quarantine pest for Argentina (SENASA, personal communication, 2008).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Last updated: 30 Jun 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

BeninPresent
Côte d'IvoirePresent
EgyptPresent
EthiopiaPresent
GuineaPresent
KenyaPresentIntroduced1976Invasive
MadagascarPresent
MauritiusPresent
MayottePresent
MoroccoPresent
NigeriaPresent
RéunionPresent
SenegalPresent, Widespread
South AfricaPresent, Few occurrences
SudanPresent1985
TanzaniaPresent
TunisiaPresent, Localized1992
ZambiaPresent
ZimbabwePresent

Asia

CambodiaAbsent, Unconfirmed presence record(s)
ChinaPresent
-AnhuiPresent
-FujianPresent
-GuangdongPresent
-GuangxiPresent
-HainanPresent
-HebeiPresent
-HenanPresent
-HubeiPresent
-JiangsuPresent
-ShandongPresent
-ShanghaiPresent
-ZhejiangPresent
IndiaPresent
-Andhra PradeshPresent1991
-DelhiPresent
-GujaratPresent
-HaryanaPresent
-Jammu and KashmirPresent
-KarnatakaPresent
-KeralaPresent
-Madhya PradeshPresent
-MaharashtraPresent
-OdishaPresent
-PunjabPresent
-Tamil NaduPresent
-TelanganaPresent
-Uttar PradeshPresent
-West BengalPresent
IndonesiaPresent
IranPresent, Widespread
IsraelPresent, Widespread
JapanPresent
-HonshuPresent
-KyushuPresent
JordanPresent
LaosAbsent, Unconfirmed presence record(s)
LebanonPresent
MalaysiaAbsent, Unconfirmed presence record(s)
OmanPresent
PhilippinesPresent
Saudi ArabiaPresent
South KoreaPresent
TaiwanPresent, Few occurrences
ThailandAbsent, Unconfirmed presence record(s)
TurkeyPresent, Localized1985
United Arab EmiratesPresent
VietnamPresent, Localized
YemenPresent

Europe

AustriaPresent, LocalizedFirst reported: 198*
BelgiumPresent, Localized
Bosnia and HerzegovinaPresent
BulgariaAbsent, Eradicated1985
CroatiaPresent, Localized
CyprusPresent, Widespread1988
CzechiaAbsent, Eradicated1981
DenmarkAbsent, Intercepted only
EstoniaAbsent, Confirmed absent by survey
FinlandPresent, Few occurrences
FrancePresent, Widespread
GermanyAbsent, Formerly presentFirst reported: 197*
GreecePresent, Localized
-CretePresent
HungaryAbsent, Eradicated1986
IrelandAbsent, Eradicated
ItalyPresent, Widespread1979
-SardiniaPresent
-SicilyPresent
LithuaniaAbsent, Confirmed absent by survey
MaltaPresent
MoldovaPresent
MontenegroAbsent, Formerly present
NetherlandsPresent, Localized1976
NorwayAbsent, Eradicated
PolandAbsent, Formerly present1980
PortugalPresent, Localized
RomaniaPresent, Few occurrences
RussiaPresent, Localized
-Central RussiaPresent, Localized
-Southern RussiaPresent, Few occurrences
SerbiaPresent
Serbia and MontenegroPresent, Localized
SlovakiaAbsent, Invalid presence record(s)
SloveniaAbsent, Eradicated
SpainPresent, Widespread
-Canary IslandsPresent, Localized
SwedenAbsent, Eradicated1980
SwitzerlandPresent, Few occurrencesFirst reported: 198*
United KingdomAbsent, Eradicated1977
-EnglandAbsent, Eradicated

North America

BahamasPresent
BarbadosPresent
BermudaPresent
British Virgin IslandsPresent
CanadaPresent, Localized
-AlbertaPresent
-Nova ScotiaPresent
-OntarioPresent
-QuebecPresent
Costa RicaPresent
CubaPresent
Dominican RepublicPresent
GuadeloupePresent
GuatemalaPresent
MartiniquePresent, Widespread
MexicoPresent
Netherlands AntillesPresent, Localized
Puerto RicoPresent
Saint Kitts and NevisPresent, Localized
Trinidad and TobagoPresent
U.S. Virgin IslandsPresent
United StatesPresent, Localized
-ArizonaPresent
-CaliforniaPresent
-DelawarePresent
-District of ColumbiaPresent
-FloridaPresent
-HawaiiPresent
-IndianaPresent
-IowaPresent
-MarylandPresent
-MassachusettsPresent
-MichiganPresent
-NebraskaPresent
-New JerseyPresent
-New MexicoPresent
-OhioPresent
-PennsylvaniaPresent
-South CarolinaPresent
-TexasPresent
-WashingtonPresent
-WisconsinPresent

Oceania

American SamoaPresent
AustraliaAbsent, Intercepted only
-New South WalesAbsent, Intercepted only
-VictoriaAbsent, Intercepted only
Federated States of MicronesiaPresent
GuamPresent
Northern Mariana IslandsPresent
SamoaPresent
TongaPresent

South America

ArgentinaAbsent, Unconfirmed presence record(s)Original citation: SENASA, personal communication, 2008
BrazilPresent
-Minas GeraisPresent
-PernambucoPresent
-Rio Grande do NortePresent
-Sao PauloPresent
ChilePresent, Localized
ColombiaPresent
EcuadorPresent
French GuianaPresent
GuyanaPresent
PeruPresent
VenezuelaPresent

Risk of Introduction

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L. trifolii is listed as an A2 quarantine pest by EPPO (OEPP/EPPO, 1984). It is one of the most important recent introductions to the EPPO region.

It is a major pest of a wide variety of ornamental or vegetable crops grown under glass (Lactuca, Dendranthema, Gypsophila, Dahlia) or as protected crops in the EPPO region. It could also cause damage to these crops grown in the open in the warmer parts of the EPPO region. It is widely distributed in the region and the success of eradication programmes which have been conducted cannot be confirmed.

Habitat

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L. trifolii'sdevelopment is strictly connected with temperature. Consequently, at a uniform temperature of 28°C one generation cycle can be accomplished in 14-15 days, but at lower temperatures the time taken is progressively longer. At 16°C puparial diapause begins and winter generations of puparia will remain in the soil until warmer conditions occur again. The adult can survive temperatures down to about 12°C but does not appear to feed or lay eggs.

In heated glasshouses where suitable hosts may be grown throughout the year, the breeding and development of L. trifolii will be virtually continuous. In cool glasshouses generation rates will be different throughout the seasons, with fairly rapid development during the summer and puparia remaining undeveloped in the soil during the coldest periods.

In the moderate and variable temperatures of open-field cultivation there will be only a few (perhaps three) generations produced throughout the growing season because of the longer time required to complete each cycle (Süss et al., 1984).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial

Hosts/Species Affected

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The host range of L. trifolii includes over 400 species of plants in 28 families including both ornamental crops (Bogran, 2006) and vegetables (Cheri, 2012). The main host families and species include: Apiaceae (A. graveolens); Asteraceae (Aster spp., Chrysanthemum spp., Gerbera spp., Dahlia spp., Ixeris stolonifera, Lactuca sativa, Lactuca spp., Zinnia spp.); Brassicaceae (Brassica spp.); Caryophyllaceae (Gypsophila spp.); Chenopodiaceae (Spinacia oleracea, Beta vulgaris); Cucurbitaceae (Cucumis spp., Cucurbita spp.); Fabaceae (Glycine max, Medicago sativa, Phaseolus vulgaris, Pisum sativum, Pisum spp., Trifolium spp., Vicia faba); Liliaceae (A. cepa, Allium sativum) and Solanaceae (Capsicum annuum, Capsicum frutescens, Petunia spp., Solanum lycopersicum, Solanum spp.) (EFSA, 2012).

It is now considered to be the most important pest of cowpea (Vigna uniguilata), towel gourd (Luffa cylindrica), cucumber (Cucumis sativus) and many other vegetable crops in southern China (Gao, 2014). In Europe, L. trifolii is a major pest of lettuce, beans, cucumber and celery, Capsicum sp., carnations, clover, Gerbera sp., Gypsophila sp., lucerne, Senecio hybridus, potatoes and tomatoes (EFSA, 2012). It is now a major pest of the Compositae worldwide, particularly chrysanthemums (including Dendranthenum, the commercial 'Mum') in North America, Colombia, and elsewhere. It also causes severe damage to different open field crops, such as chili peppers in Mexico.

Host Plants and Other Plants Affected

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Plant nameFamilyContextReferences
Abelmoschus esculentus (okra)MalvaceaeMain
    AgeratumAsteraceaeMain
      AlliumLiliaceaeMain
        Allium cepa (onion)LiliaceaeOther
          Allium sativum (garlic)LiliaceaeMain
            Allium schoenoprasum (chives)LiliaceaeOther
              Alstroemeria (Inca lily)AlstroemeriaceaeWild host
                Ambrosia (Ragweed)AsteraceaeWild host
                  Antirrhinum (snapdragon)ScrophulariaceaeWild host
                    Apium graveolens var. dulce (celery)ApiaceaeOther
                      ArachisFabaceaeWild host
                        Arachis hypogaea (groundnut)FabaceaeMain
                          Artemisia (wormwoods)AsteraceaeWild host
                            AsterAsteraceaeMain
                              Avena sativa (oats)PoaceaeWild host
                                BaccharisAsteraceaeWild host
                                  BasellaBasellaceaeWild host
                                    BellisAsteraceaeOther
                                      Beta vulgaris var. saccharifera (sugarbeet)ChenopodiaceaeMain
                                        Bidens (Burmarigold)AsteraceaeMain
                                          Brassica rapa cultivar group MizunaBrassicaceaeMain
                                            Brassica rapa subsp. chinensis (Chinese cabbage)BrassicaceaeMain
                                              CallistephusAsteraceaeMain
                                                Capsicum annuum (bell pepper)SolanaceaeMain
                                                  CarthamusAsteraceaeWild host
                                                    Cassia (sennas)FabaceaeOther
                                                      Centaurea (Knapweed)AsteraceaeOther
                                                        Cestrum (jessamine)SolanaceaeWild host
                                                          Chenopodium (Goosefoot)ChenopodiaceaeOther
                                                            Chrysanthemum (daisy)AsteraceaeMain
                                                              Chrysanthemum indicum (chrysanthemum)AsteraceaeOther
                                                                Chrysanthemum morifolium (chrysanthemum (florists'))AsteraceaeMain
                                                                  CitrullusCucurbitaceaeOther
                                                                    Citrullus lanatus (watermelon)CucurbitaceaeOther
                                                                      Coffea arabica (arabica coffee)RubiaceaeOther
                                                                        Coffea canephora (robusta coffee)RubiaceaeOther
                                                                          Crataegus (hawthorns)RosaceaeWild host
                                                                            CrotalariaFabaceaeWild host
                                                                              Cucumis melo (melon)CucurbitaceaeMain
                                                                                Cucumis sativus (cucumber)CucurbitaceaeMain
                                                                                  Cucurbita maxima (giant pumpkin)CucurbitaceaeOther
                                                                                    Cucurbita moschata (pumpkin)CucurbitaceaeOther
                                                                                      Cucurbita pepo (marrow)CucurbitaceaeMain
                                                                                        Cucurbitaceae (cucurbits)CucurbitaceaeMain
                                                                                          DahliaAsteraceaeMain
                                                                                            Daucus carota (carrot)ApiaceaeOther
                                                                                              Dianthus (carnation)CaryophyllaceaeMain
                                                                                                Erigeron (Fleabane)AsteraceaeOther
                                                                                                  EupatoriumAsteraceaeWild host
                                                                                                    GaillardiaAsteraceaeMain
                                                                                                      Gazania (treasure-flower)AsteraceaeOther
                                                                                                        Gerbera (Barbeton daisy)AsteraceaeMain
                                                                                                          Gladiolus hybrids (sword lily)IridaceaeOther
                                                                                                            GlycineFabaceaeOther
                                                                                                              Glycine max (soyabean)FabaceaeMain
                                                                                                                Gossypium (cotton)MalvaceaeMain
                                                                                                                  Gypsophila (baby's breath)CaryophyllaceaeMain
                                                                                                                    Helianthus (sunflower)AsteraceaeMain
                                                                                                                      Hordeum (barleys)PoaceaeOther
                                                                                                                        Ipomoea (morning glory)ConvolvulaceaeWild host
                                                                                                                          Lactuca sativa (lettuce)AsteraceaeMain
                                                                                                                            Lagenaria siceraria (bottle gourd)CucurbitaceaeOther
                                                                                                                              Lathyrus (Vetchling)FabaceaeMain
                                                                                                                                Linaria (Toadflax)ScrophulariaceaeOther
                                                                                                                                  Luffa acutangula (angled luffa)CucurbitaceaeOther
                                                                                                                                    Luffa aegyptiaca (loofah)CucurbitaceaeOther
                                                                                                                                      LycopersiconSolanaceaeMain
                                                                                                                                        MacrotylomaFabaceaeOther
                                                                                                                                          Malva (mallow)MalvaceaeWild host
                                                                                                                                            Medicago (medic)FabaceaeOther
                                                                                                                                              Medicago sativa (lucerne)FabaceaeMain
                                                                                                                                                Melilotus (melilots)FabaceaeWild host
                                                                                                                                                  MollucellaWild host
                                                                                                                                                    OcimumLamiaceaeWild host
                                                                                                                                                      Phaseolus (beans)FabaceaeMain
                                                                                                                                                        Phaseolus lunatus (lima bean)FabaceaeMain
                                                                                                                                                          Phaseolus vulgaris (common bean)FabaceaeMain
                                                                                                                                                            PhloxPolemoniaceaeWild host
                                                                                                                                                              Physalis (Groundcherry)SolanaceaeWild host
                                                                                                                                                                Pisum sativum (pea)FabaceaeMain
                                                                                                                                                                  Polyphagous (polyphagous)Main
                                                                                                                                                                    Primula (Primrose)PrimulaceaeOther
                                                                                                                                                                      RicinusEuphorbiaceaeWild host
                                                                                                                                                                        Ricinus communis (castor bean)EuphorbiaceaeOther
                                                                                                                                                                          Salvia (sage)LamiaceaeMain
                                                                                                                                                                            Senecio (Groundsel)AsteraceaeMain
                                                                                                                                                                              Solanum lycopersicum (tomato)SolanaceaeMain
                                                                                                                                                                                Solanum melongena (aubergine)SolanaceaeMain
                                                                                                                                                                                  Solanum tuberosum (potato)SolanaceaeMain
                                                                                                                                                                                    Sonchus (Sowthistle)AsteraceaeWild host
                                                                                                                                                                                      Spinacia oleracea (spinach)ChenopodiaceaeMain
                                                                                                                                                                                        Tagetes (marigold)AsteraceaeMain
                                                                                                                                                                                          Taraxacum (dandelion)AsteraceaeWild host
                                                                                                                                                                                            TithoniaAsteraceaeWild host
                                                                                                                                                                                              Tragopogon (goat's-beard)AsteraceaeWild host
                                                                                                                                                                                                Tribulus (caltrop)ZygophyllaceaeWild host
                                                                                                                                                                                                  Trifolium (clovers)FabaceaeMain
                                                                                                                                                                                                    Trifolium repens (white clover)FabaceaeMain
                                                                                                                                                                                                      TrigonellaFabaceaeWild host
                                                                                                                                                                                                        TropaeolumTropaeolaceaeMain
                                                                                                                                                                                                          Typha (reedmace)TyphaceaeWild host
                                                                                                                                                                                                            Verbena (vervain)VerbenaceaeWild host
                                                                                                                                                                                                              Vicia (vetch)FabaceaeMain
                                                                                                                                                                                                                Vicia faba (faba bean)FabaceaeOther
                                                                                                                                                                                                                  Vigna unguiculata (cowpea)FabaceaeMain
                                                                                                                                                                                                                    Xanthium (Cocklebur)AsteraceaeOther
                                                                                                                                                                                                                      ZinniaAsteraceaeMain

                                                                                                                                                                                                                        Growth Stages

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                                                                                                                                                                                                                        Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

                                                                                                                                                                                                                        Symptoms

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                                                                                                                                                                                                                        L. trifolii feeding punctures appear as white speckles between 0.13 and 0.15 mm in diameter. Oviposition punctures are usually smaller (0.05 mm) and are more uniformly round.

                                                                                                                                                                                                                        L. trifolii leaf mines can vary in form with the host plant, but when adequate leaf area is available they are usually long, linear, narrow and not greatly widening towards the end. They are usually greenish white.

                                                                                                                                                                                                                        In very small leaves the limited area for feeding results in the formation of a secondary blotch at the end of the mine, before pupariation. In Kenya, Spencer (1985) notes the growth of many L. trifolii from mines which began with a conspicuous spiral. This is not a characteristic associated with L. trifolii on other continents.

                                                                                                                                                                                                                        The frass is distinctive in being deposited in black strips alternately at either side of the mine (like L. sativae), but becomes more granular towards the end of the mine (unlike L. sativae) (Spencer, 1973).

                                                                                                                                                                                                                        Fungal destruction of the leaf may also occur as a result of infection introduced by L. trifolii from other sources during breeding activity. Wilt may occur, especially in seedlings.

                                                                                                                                                                                                                        List of Symptoms/Signs

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                                                                                                                                                                                                                        SignLife StagesType
                                                                                                                                                                                                                        Leaves / abnormal colours
                                                                                                                                                                                                                        Leaves / abnormal forms
                                                                                                                                                                                                                        Leaves / abnormal leaf fall
                                                                                                                                                                                                                        Leaves / external feeding
                                                                                                                                                                                                                        Leaves / internal feeding
                                                                                                                                                                                                                        Leaves / necrotic areas
                                                                                                                                                                                                                        Leaves / wilting

                                                                                                                                                                                                                        Biology and Ecology

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                                                                                                                                                                                                                        Egg

                                                                                                                                                                                                                        L. trifolii eggs are inserted just below the leaf surface. Eggs hatch in 2-5 days according to temperature. Harris and Tate (1933) give 4-7 days at 24°C. Many eggs may be laid on a single leaf.

                                                                                                                                                                                                                        Larva

                                                                                                                                                                                                                        The duration of larval development also depends on temperature and probably host plant. Several generations can occur during the year, breeding only being restricted by the temperature and the availability of fresh plant growth in suitable hosts (Spencer, 1973).

                                                                                                                                                                                                                        Puparium

                                                                                                                                                                                                                        L. trifolii pupariation occurs outside the leaf, in the soil beneath the plant. Puparial development will vary according to season and temperature. Adult emergence occurs 7-14 days after pupariation at temperatures between 20 and 30°C (Leibee, 1982). Wolfenbarger (1947) gives 24-28 days for the complete cycle, in Florida during December-January (winter period).

                                                                                                                                                                                                                        Adult

                                                                                                                                                                                                                        Peak emergence of adult L. trifolii occurs before midday (McGregor, 1914). Males usually emerge before females. Mating takes place from 24 hours after emergence and a single mating is sufficient to fertilize all a female's eggs.

                                                                                                                                                                                                                        Female L. trifolii flies puncture the leaves of the host plants causing wounds which serve as sites for feeding or oviposition. Feeding punctures cause the destruction of a large number of cells and are clearly visible to the naked eye. About 15% of oviposition punctures made by L. trifolii contain viable eggs (Parrella et al., 1981). Male L. trifolii are unable to puncture the leaves but have been observed feeding at punctures made by females. Both male and female L. trifolii feed on dilute honey (in the laboratory) and take nectar from flowers (OEPP/EPPO, 1990).

                                                                                                                                                                                                                        In the southern USA, the L. trifolii 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 generations followed by a number of incomplete, overlapping generations (Spencer, 1973).

                                                                                                                                                                                                                        On celery L. trifolii completes its life cycle (oviposition to adult emergence) in 12 days at 35°C, 26 days at 20°C, and 54 days at 15°C (Leibee, 1982). On chrysanthemums the life-cycle is completed in 24 days at 20°C but on Vigna sinensis and Phaseolus lunatus it takes only 20 days at this temperature (Poe, 1981).

                                                                                                                                                                                                                        Adults of L. trifolii live between 15 and 30 days. On average, females live longer than males.

                                                                                                                                                                                                                        Both male and female L. trifolii may act as vectors for disease by transference during feeding or egg laying, but are not inherent carriers of disease.

                                                                                                                                                                                                                        Natural enemies

                                                                                                                                                                                                                        Top of page
                                                                                                                                                                                                                        Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
                                                                                                                                                                                                                        Bacillus thuringiensis kurstaki Pathogen
                                                                                                                                                                                                                        Beauveria bassiana Pathogen
                                                                                                                                                                                                                        Chrysocharis ainsliei Parasite
                                                                                                                                                                                                                        Chrysocharis caribea Parasite Arthropods|Larvae
                                                                                                                                                                                                                        Chrysocharis clarkae Parasite Hawaii; USA chrysanthemums
                                                                                                                                                                                                                        Chrysocharis giraulti Parasite Hawaii chrysanthemums
                                                                                                                                                                                                                        Chrysocharis melaensis Parasite Hawaii chrysanthemums
                                                                                                                                                                                                                        Chrysocharis oscinidis Parasite Arthropods|Larvae USA; Hawaii; Senegal chrysanthemums; okras; potatoes; Solanum aethiopicum; vegetables ì ì
                                                                                                                                                                                                                        Chrysocharis pentheus Parasite
                                                                                                                                                                                                                        Chrysocharis punctiventris Parasite
                                                                                                                                                                                                                        Chrysonotomyia okazakii Parasite
                                                                                                                                                                                                                        Chrysonotomyia punctiventris Parasite Arthropods|Larvae Hawaii; Senegal; USA; Hawaii chrysanthemums; okras; potatoes; Solanum aethiopicum; watermelons
                                                                                                                                                                                                                        Cirrospilus vittatus Parasite
                                                                                                                                                                                                                        Cirrospilus vittatus Parasite
                                                                                                                                                                                                                        Closterocerus purpureus Parasite Arthropods|Larvae
                                                                                                                                                                                                                        Closterocerus trifasciatus Parasite Arthropods|Larvae
                                                                                                                                                                                                                        Closterocerus utahensis Parasite USA; Hawaii watermelons
                                                                                                                                                                                                                        Cothonaspis pacifica Parasite Guam; USA; Hawaii Phaseolus vulgaris; Vigna unguiculata; watermelons
                                                                                                                                                                                                                        Dacnusa sibirica Parasite Netherlands tomatoes
                                                                                                                                                                                                                        Diaulinopsis callichroma Parasite Hawaii; Senegal; Trinidad and Tobago aubergines; chrysanthemums; okras; potatoes; Solanum aethiopicum; tomatoes
                                                                                                                                                                                                                        Dicyphus tamaninii Predator
                                                                                                                                                                                                                        Diglyphus begini Parasite Arthropods|Larvae California; Colombia; Guam; Hawaii; USA; Hawaii beans; chrysanthemums; watermelons
                                                                                                                                                                                                                        Diglyphus chabrias Parasite
                                                                                                                                                                                                                        Diglyphus intermedius Parasite Arthropods|Larvae Hawaii; Senegal; USA; USA; California chrysanthemums; Gerbera; okras; potatoes; Solanum aethiopicum
                                                                                                                                                                                                                        Diglyphus isaea Parasite Arthropods|Larvae Hawaii; Netherlands; Poland chrysanthemums; tomatoes
                                                                                                                                                                                                                        Diglyphus minoeus Parasite Barbados vegetables
                                                                                                                                                                                                                        Diglyphus pulchripes Parasite Hawaii; USA chrysanthemums
                                                                                                                                                                                                                        Epiclerus nomocerus Parasite
                                                                                                                                                                                                                        Eucoilidea fetura Parasite
                                                                                                                                                                                                                        Eucoilidea guamensis Parasite Guam Phaseolus vulgaris; Vigna unguiculata
                                                                                                                                                                                                                        Eucoilidea micromorpha Parasite Guam Phaseolus vulgaris; Vigna unguiculata
                                                                                                                                                                                                                        Ganaspidium hunteri Parasite Arthropods|Larvae Hawaii; USA; Hawaii chrysanthemums; watermelons
                                                                                                                                                                                                                        Ganaspidium utilis Parasite Arthropods|Larvae Guam; Tonga beans; vegetables
                                                                                                                                                                                                                        Gnaptodon pumilio Parasite Poland chrysanthemums
                                                                                                                                                                                                                        Halticoptera Parasite Aamer and Hegazi (2014)
                                                                                                                                                                                                                        Halticoptera circulus Parasite Arthropods|Larvae Hawaii; Senegal; Trinidad and Tobago; USA; Hawaii chrysanthemums; okras; potatoes; Solanum aethiopicum; watermelons
                                                                                                                                                                                                                        Hemiptarsenus semialbiclavus Parasite
                                                                                                                                                                                                                        Hemiptarsenus varicornis Parasite Arthropods|Larvae
                                                                                                                                                                                                                        Hemiptarsenus zilahisebessi Parasite
                                                                                                                                                                                                                        Metarhizium anisopliae Pathogen
                                                                                                                                                                                                                        Neochrysocharis formosa Parasite Arthropods|Larvae Guam; Hawaii
                                                                                                                                                                                                                        Neochrysocharis okazakii Parasite
                                                                                                                                                                                                                        Neochrysocharis punctiventris Parasite
                                                                                                                                                                                                                        Nordlanderia plowa
                                                                                                                                                                                                                        Oenonogastra microrhopalae Parasite
                                                                                                                                                                                                                        Opius bruneipes Parasite
                                                                                                                                                                                                                        Opius dimidiatus Parasite Arthropods|Larvae Hawaii; Netherlands; Senegal; USA chrysanthemums; okras; potatoes; Solanum aethiopicum; tomatoes
                                                                                                                                                                                                                        Opius dissitus Parasite Arthropods|Larvae Hawaii; Senegal; USA; Hawaii chrysanthemums; okras; potatoes; Solanum aethiopicum; watermelons
                                                                                                                                                                                                                        Opius montanus Parasite Hawaii chrysanthemums
                                                                                                                                                                                                                        Opius pallipes Parasite Netherlands tomatoes
                                                                                                                                                                                                                        Orius dissitus Predator
                                                                                                                                                                                                                        Paecilomyces farinosus Pathogen
                                                                                                                                                                                                                        Paecilomyces fumosoroseus Pathogen
                                                                                                                                                                                                                        Pediobius acantha Parasite Hawaii chrysanthemums
                                                                                                                                                                                                                        Pseudopezomachus masii Parasite Aamer and Hegazi (2014)
                                                                                                                                                                                                                        Rhizarcha lestes Parasite Poland chrysanthemums
                                                                                                                                                                                                                        Steinernema carpocapsae Parasite Eggs
                                                                                                                                                                                                                        Steinernema feltiae Parasite
                                                                                                                                                                                                                        Zagrammosoma Parasite Aamer and Hegazi (2014)

                                                                                                                                                                                                                        Notes on Natural Enemies

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                                                                                                                                                                                                                        Numerous parasitic wasps (Hymenoptera) occurring naturally, may be used for control of L. trifolii. These wasps are difficult to isolate or identify and local agricultural advisory services should be consulted about which species are available and natural in that locality, and their artificial introduction.

                                                                                                                                                                                                                        There has been considerable work on natural enemies in relation to biological control introduction programmes. Waterhouse and Norris (1987) give a detailed list of the natural enemies of Liriomyza spp. and a summary of the results of the biological control introductions against L. trifolii.

                                                                                                                                                                                                                        Foliar applications of the entomophagous nematode, Steinernema carpocapsae, significantly reduced adult development of L. trifolii (Harris et al., 1990).

                                                                                                                                                                                                                        Pathway Vectors

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                                                                                                                                                                                                                        VectorNotesLong DistanceLocalReferences
                                                                                                                                                                                                                        Clothing, footwear and possessionsLand/sea/air. Yes
                                                                                                                                                                                                                        Land vehiclesRoad transport/air. Yes

                                                                                                                                                                                                                        Plant Trade

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                                                                                                                                                                                                                        Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
                                                                                                                                                                                                                        Leaves eggs; larvae Yes Pest or symptoms usually visible to the naked eye
                                                                                                                                                                                                                        Seedlings/Micropropagated plants eggs; larvae Yes Pest or symptoms usually visible to the naked eye
                                                                                                                                                                                                                        Plant parts not known to carry the pest in trade/transport
                                                                                                                                                                                                                        Bark
                                                                                                                                                                                                                        Bulbs/Tubers/Corms/Rhizomes
                                                                                                                                                                                                                        Flowers/Inflorescences/Cones/Calyx
                                                                                                                                                                                                                        Growing medium accompanying plants
                                                                                                                                                                                                                        Roots
                                                                                                                                                                                                                        Stems (above ground)/Shoots/Trunks/Branches
                                                                                                                                                                                                                        True seeds (inc. grain)
                                                                                                                                                                                                                        Wood

                                                                                                                                                                                                                        Impact

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                                                                                                                                                                                                                        L. trifolii is an economically important key pest of both ornamental crops (Bogran, 2006) and vegetables (Cheri, 2012).

                                                                                                                                                                                                                        In Kenya, chrysanthemums were grown commercially before 1976, but L. trifolii was thought to have been introduced in contaminated cuttings from Florida (USA) in 1976, at a large propagating nursery at Masongaleni. By 1979 the nursery was closed, but the establishment of the pest in local wild hosts, and the dissemination of cuttings from the nursery to other parts of the country as well as abroad, has added L. trifolii to the other pests of East Africa. It has caused considerable crop losses and loss of overseas markets due to quarantine requirements (IPPC Secretariat, 2005).

                                                                                                                                                                                                                        Vegetable losses in the USA are also considerable. For example, losses for celery were estimated at US$ 9 million in 1980 (Spencer, 1982). It was noted, however, that damage to celery during the first 2 months of the 3-month growing season was insignificant and largely cosmetic, whereas considerable yield loss resulted from pest presence during the final month (Foster et al., 1988). 1.5 million larval mines per hectare were recorded from onions in Iowa (Harris et al., 1933).

                                                                                                                                                                                                                        Damage is caused by L. trifolii larvae mining into leaves and petiole. The photosynthetic ability of the plants is often greatly reduced as the chlorophyll-containing cells are destroyed. 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 caused by L. trifolii in the leaf palisade of ornamental plants, such as chrysanthemums, can further reduce plant value (Smith et al., 1962; Musgrave et al., 1975). In young plants and seedlings, L. trifolii mining may cause considerable delay in plant development, even leading to plant loss. The level of damage depends on many factors, including climate suitability, host resistance, crop distribution, growing conditions, control methods in place and the degree of infestation (EFSA, 2012).

                                                                                                                                                                                                                        L. trifolii is also known to be a vector of plant viruses (Zitter et al., 1980).

                                                                                                                                                                                                                        Detection and Inspection

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                                                                                                                                                                                                                        L. trifolii are small black and yellow flies which may be detected flying closely around host plants or moving erratically and rapidly upon the leaf surfaces. Inspection of the leaf surface will reveal punctures of the epidermis and the obvious greenish-white mines with linear grains of frass along their length. For accurate identification, examination of the leaf mine and all stages of development are crucial.

                                                                                                                                                                                                                        L. trifolii larvae will be found feeding at the end of the mine, or the mine will end with a small convex slit in the epidermis where the larva has left the mine to pupariate on the ground. Sometimes the puparium may be found adhering to the leaf surface, although in most cases the fully-fed larva will have found its way to the ground beneath the plant to pupariate. This is especially true in hot, dry conditions where the larva/puparia would quickly desiccate if exposed on the leaf surface. Empty puparial cases are split at the anterior end, but the head capsule is not usually separated from the rest of the case.

                                                                                                                                                                                                                        Mined leaves should be collected into polythene bags and transferred to a press as soon as possible. Leaves containing larvae intended for breeding should be collected into individual polythene bags, which on return to the laboratory should be slightly over-pressurized by blowing into them before sealing the end. Blowing up the bag by mouth and sealing it adds valuable carbon dioxide to the moist air mix. Constant attention is required to ensure that puparia are transferred to individual tubes until the fly emerges. If the plant material begins rotting, good material with feeding larvae must be removed to more sanitary conditions.

                                                                                                                                                                                                                        When puparia are observed they can be very carefully removed to tubes containing a layer of fine sand, or a small strip of blotting paper or filter paper. This should be kept damp (never wet) until the adult emerges.

                                                                                                                                                                                                                        On emergence, the fly should be kept for at least 24 hours to harden up. Do not allow condensation to come into contact with the fly, or it will stick to the water film and be damaged.

                                                                                                                                                                                                                        Field collection of the adult L. trifolii is done by netting. The use of sticky traps, especially yellow ones, placed near host plants is a very effective method of collection and estimation of infestation.

                                                                                                                                                                                                                        If the puparial stage is collected from the soil, care must be taken not to damage the puparial skin or death will almost certainly follow. The pupae should be stored in glass tubes on a layer of clean sand or, better still, thick filter paper. The tube must have high humidity, but be free of condensation.

                                                                                                                                                                                                                        When the fly emerges, it must be allowed to harden for 24 hours before killing for identification purposes. Ensure that the tube has no condensation present.

                                                                                                                                                                                                                        Newly emerged adult L. trifolii are generally softer than specimens aged for several days and may crinkle as drying proceeds, especially the head. The ptilinal sac may still protrude from the suture between the frons and face obliterating some important characteristics. Adults should be dried slowly in the dark in a sealed receptacle over blotting paper. If preserving wet is preferred, the live specimen should be dropped into 20-40% alcohol, and transferred to 70-90% alcohol after 2 days.

                                                                                                                                                                                                                        Similarities to Other Species/Conditions

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                                                                                                                                                                                                                        Liriomyza species, in general, may be recognized by their black (sometimes brilliantly black) and yellow colouring. Particularly, the scutellum is usually yellow and distinctive.

                                                                                                                                                                                                                        Several pests in this genus are similar and may be mistaken for each other on quick examination. These are L. sativae (shining black mesonotum without yellow at the hindquarters, vte always and vti usually on black ground, origins probably in South America); L. huidobrensis (which has a larger discal cell, origins in South America); L. trifolii (origins probably Caribbean/Florida); L. brassicae (origins probably South America/Caribbean); L. bryoniae (origins in Europe); L. congesta (Origins in Europe/western Asia); L. strigata (origins in Europe).

                                                                                                                                                                                                                        The spread of Liriomyza species through international commerce and the similarities between the seven species means that identification of individual infestations must be confirmed by specialists (Spencer, 1973).

                                                                                                                                                                                                                        Prevention and Control

                                                                                                                                                                                                                        Top of page

                                                                                                                                                                                                                        Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

                                                                                                                                                                                                                        Physical Control

                                                                                                                                                                                                                        The use of glue traps can be effective for assessing the presence of adult L. trifolii, gauging the best time to apply control measures on a population, and as a direct method of pest suppression (Valenzuela, 2010). Yellow sticky traps (YSTs) attracted significantly more adult L. trifolii than blue, purple or white traps; the average percentage of damaged leaves and damage severity (number of mines per leaf) were significantly lower in fields with YSTs after 50 days (Arida et al., 2013).

                                                                                                                                                                                                                        Chemical Control

                                                                                                                                                                                                                        L. trifolii has developed resistance to most commonly used insecticides that were recommended for its control before 1990 (Parella et al., 1984; Nuessly and Webb, 2013), including carbamates, organophosphates, pyrethroids, avermectins, spinosyns and moulting disruptors, such as cyromazina (Hernandez, 2009). However, its susceptibility to insecticides varies widely between agricultural regions and populations. In Florida, USA, the lifetime of an insecticide’s effectiveness is often only two to four years, and is then usually followed by a strong resistance in treated populations (Reitz et al., 2013; Capinera, 2014).

                                                                                                                                                                                                                        The insecticides (active ingredients) abamectin, acephate, acephate + fenpropathrin, acetamiprid, bifenazate + abamectin, bifenthrin, carbaryl, chlorpyrifos, clothianidin, cyantraniliprole, cyromazine, deltamethrin, diazinon, diflubenzuron, dimethoate, dinotefuran, emamectin benzoate, fenpropathrin, fenoxycarb, gamma-cyhalothrin, imidacloprid, indoxacarb, lambda-cyhalothrin, lambda-cyhalothrin + chlorantraniliprole, malathion, novaluron, naled, permethrin, phosmet, rynaxypyr (chlorantraniliprole), spinetoram, spinosad, thiamethoxam, thiamethoxam + chlorantraniliprole, and the natural insecticides azadirachtin, extract of Chenopodium ambrosioides, Isaria fumosorosea Apopka strain 97, mineral oils, potassium salts of fatty acids and pyrethrins have been cited for the control or suppression of immature or adult L. trifolii in agricultural and ornamental crops (Price and Nagle, 2012; Webb et al., 2012; Webb and Stansly, 2012; Misra, 2013; Nuessly and Webb, 2013; Webb, 2013).

                                                                                                                                                                                                                        For the control of L. trifolii, effective insecticides with different modes of action (and with different site of action) should be rotated during the growing season (IRAC, 2014).

                                                                                                                                                                                                                        Biological Control

                                                                                                                                                                                                                        Natural enemies periodically suppress leaf-miner populations (Spencer, 1972). Parasitoids, and to a lesser extent to nematodes, bacteria and fungi, are used for biological control of leafminers (Cikman y Comelkcloglu, 2006; Sher et al. 2000; Abd El-Salam et al., 2012; Capinera, 2014). Although several predatory species have been found feeding on Liriomyza, predators are not considered to be important as biological control agents (Liu et al., 2009; Capinera 2011, 2014). There are several successful cases of classical biological control with parasitoids to different species of leaf miners, both in open fields and greenhouses (Abd-Rabou, 2006; Salvo y Valladares, 2007; Liu et al., 2011;).

                                                                                                                                                                                                                        There has been considerable work on natural enemies in relation to biological control introduction programmes. Waterhouse and Norris (1987) gave a detailed list of the natural enemies of Liriomyza spp. and a summary of the results of the biological control introductions against L. trifolii. In Hawaii, several parasitoids were already present as immigrant species, presumably accidentally introduced with their hosts. More of these parasitoids were introduced from the USA, to broaden the genetic base, as well as Chrysonotomyia punctiventris and Ganaspidium hunteri, and have proved a substantial control, at least on water melons when natural enemies are not eliminated by pesticide sprays (Johnson, 1987). Subsequently, introductions of species established in Hawaii were made in Pohnpei (Mariana Islands) and G. utilis and C. oscinidis became established and are credited with achieving substantial control (Suta and Esguerra, 1993). These two parasitoids have also been successfully established in Tonga where control is reported as complete (Johnson, 1993). Earlier unsuccessful introductions were made in the Caribbean islands (Cock, 1985) and a biological control programme has been carried out in Senegal: the results of this require re-assessment but it is unlikely that any beneficial results were obtained (Neuenschwander et al., 1987).

                                                                                                                                                                                                                        Foliar applications of the entomophagous nematode Steinernema carpocapsae significantly reduced adult development of L. trifolii (Harris et al., 1990).

                                                                                                                                                                                                                        Extensive global research has reported more than 150 species of parasitoids associated with Liriomyza sp. (Liu et al. 2011). For L. trifolii,Hernandez et al. (2010) listed 20 genera of parasitoids in various chili crops during autumn 2007 and spring 2008 in Weslaco, Texas, USA: Neochrysocharis formosa, Closterocerus cinctippenis Ashmead, Diglyphus isaea, Cirrospilus variegatus Masi, Asecodes spp., Pnigalio spp., Zogrammosoma spp., Chrysocharis spp. (Eulophidae); Opius dissitus Muesebeck, O. dimidiatus (Ashmead), O. nr. brownsvillensis Fischer, O. thoracosema Fischer, O. bruneipes Gahan, O. spp. (Braconidae); Ganaspidium pusillae Weld, G. nigrimanus (=utilis) (Kieffer), Disorygma pacifica (Yoshimoto), Agrostocynips robusta (Ashmead) (Figitidae) and Halticoptera nr. circulus Walker (Pteromalidae). N. formosa was the most common, comprising 60% of the natural enemies.

                                                                                                                                                                                                                        In Tamaulipas, Mexico, Arcos-Cavazos et al. (2011) found six larval parasitoid hymenopterid natural enemies: Opius sp., Chysocharis sp., Diglyphus sp. (Eulophidae), Gronotoma sp. (Hymenoptera: Figitidae), and two unidentified species. Of these, Chrysocharis was the primary regulator of L. trifolii populations, with an average of 79.5% larval parasitism of L. trifolii and in some samples of 100%. Fadl and El-Khawas (2009) found five species of hymenopterid parasitoids of L. trifolii on tomato in Qalyubia, Egypt, during two growing crop seasons: Cirrospilus sp., Diglyphus crassinervis, D. isaea, Chrysocharis sp. and Neochrysocharis.Neochrysocharis had the highest recorded total numbers.

                                                                                                                                                                                                                        Currently, mass rearing of leaf miner parasitoids for augmentative biological control includes the simultaneous use of three trophic levels: host plant, phytophagous insects and parasitoids, which may be difficult and costly. Therefore, the idea should be carefully considered (Cortez-Mondaca and Valenzuela-Escoboza, 2013).

                                                                                                                                                                                                                        The impact of insecticides on parasitoids of leaf miners is complex and further studies are needed to determine which insecticides are least damaging to natural enemies of L. trifolii (Hernandez 2009). Field studies suggested that cyromazine has the least impact on parasitoid populations, followed by abamectin and spinosyns, which in turn were not as detrimental as carbamates, organophosphate or pyrethroids (Reitz et al., 2013). Nuessly and Webb (2013) reported that the use of selective insecticides, such as spinosad and emamectin benzoate, for armyworm and cabbage looper control also provided some control of L. trifolii populations, as well as being gentle to most beneficial insects. Novaluron had the least impact on adult parasitoids in laboratory bioassays compared to other treatments (abamectin, spinetoram, lambda-cyhalothrin) (Hernandez, 2009). The insecticide lambda-cyhalothrin showed negative effects only for the parasitoid Ganaspidium nigrimanus (in topical application assays), but residual tests had negative effects on G. nigrimanus and on Neochrysocharis formosa. Abamectin showed no ill effects on N. formosa or G. nigrimanus in topical bioassays. In contrast, spinetoram showed negative effects on N. formosa and G. nigrimanus in all bioassays in the laboratory.

                                                                                                                                                                                                                        It is possible to increase the action of leafminer natural enemies through habitat management (Musundire et al., 2012). Weed patches near crops may be important as possible reservoirs of parasitoids (Altieri and Nichols, 2009). For this reason, there have been suggestions of increasing weed diversity or improving the availability of pollen and nectar for natural enemies in agroecosystems affected by L. trifolii (Altieri et al., 2005; Altieri and Nichols, 2009). The combined use of cultural practices and low- or reduced-impact insecticides on non-target species might favour populations of parasites (Cortez-Mondaca and Valenzuela-Escoboza, 2013; Reitz et al., 2013).

                                                                                                                                                                                                                        Cultural Control

                                                                                                                                                                                                                        In chrysanthemum cuttings, L. trifolii survived cold storage at 1.7°C for at least 10 days. Newly laid eggs of L. trifolii in chrysanthemums survived for up to 3 weeks in cold storage at 0°C (Webb et al., 1970). Webb et al. (1970) therefore proposed that chrysanthemum cuttings should be maintained under normal glasshouse conditions for 3-4 days after lifting to allow eggs to hatch. Subsequent storage of plants at 0°C for 1-2 weeks should then kill the larvae.

                                                                                                                                                                                                                        Gamma irradiation of eggs and first larval stages at doses of 40-50 Gy provided effective control (Süss et al., 1986; Yathom et al., 1991). The release of sterile L. trifolii males significantly reduced the number of offspring (Kaspy and Parrella, 2006). When the release of sterile males was combined with a release of the parasitoid Diglyphus isaia, the damage caused by L. trifolii and the size of the adult population were significantly reduced.

                                                                                                                                                                                                                        It is important to destroy and bury the remains of broadleaf weeds and senescent cultures as they can harbor reproductive leaf miners (Capinera, 2011; University of California, 2012).

                                                                                                                                                                                                                        Yildrim and Unay (2011) noted that foliar fertilizers of fulvic acid and calcium nitrate combinations in tomato had a negative effect on L. trifolii population. Mortezaiefard et al. (2012) found that foliar applications of potassium silicate reduced L. trifolii populations on Gerbera jamesonii.

                                                                                                                                                                                                                        Host Plants

                                                                                                                                                                                                                        Lei et al. (2008) found that L. trifolii were found more often and made more feeding punctures on non-Bt transgenic cotton plants than on Bt cotton plants. Females oviposited more eggs on non-Bt cotton plants, but larval and puparial survival did not differ between Bt and non-Bt plants.

                                                                                                                                                                                                                        Sahu et al. (2006) reported that the leaf area of the lower leaves of the tomato plants was positively correlated with the percentage of leaves affected by L. trifolii, indicating that L. trifolii infestation increases with increasing leaf surface area. Thus, genotypes with narrow leaves would be less preferred by the species. Studies with similar purposes have been made ??in the castor oil plant Ricinus communis and cowpea Vigna unguiculata, among others (Eid, 2008; Hedge et al., 2009).

                                                                                                                                                                                                                        The nitrogen content in the leaves of a host plant of L. trifolii is an important component that influences in the susceptibility to attack (Altieri et al., 2005). Potassium and phosphorus reduce the susceptibility in potato crops and cause negative effects on pest (Minkenberg and van Lenteren, 1986; Facknath & Lalljee, 2005).

                                                                                                                                                                                                                        Integrated Pest Management

                                                                                                                                                                                                                        The selection, integration and implementation of different control tactics of the leafminer, based on the conservation of biological control, is sufficient for adequate management of L. trifolii (Liu et al., 2009, 2011; Cortez-Mondaca and Valenzuela-Escoboza, 2013). One of the most important steps is the use of selective or specific biorational insecticides, such as botanical extracts, soaps, minerals, entomopathogenic insecticides and growth regulators (Hernandez, 2009; Hernández 2011; Liu et al., 2009, 2011; Yildirim and Baspinar 2012). It is also important to apply insecticides so that they cause the least impact to natural enemies; for instance, some systemic insecticides can be applied in the seed or irrigation system (Cikman and Comelkcloglu, 2006; Nath and Singh, 2006; Kumar, 2010; El-Wakeil et al., 2013).

                                                                                                                                                                                                                        Regulatory Control

                                                                                                                                                                                                                        To avoid the introduction of L. trifolii (and other leaf miner species L. huidobrensis, L. sativae and Amauromyza maculosa [Nemorimyza maculosa]), EPPO recommends that propagating material (except seeds) of Capsicum, carnations, celery, chrysanthemums, Cucumis, Gerbera, Gypsophila, lettuces, Senecio hybridus and tomatoes from countries where L. trifolii occurs must have been inspected at least every month during the previous 3 months and found free from the pests (EOPP/EPPO, 1990).

                                                                                                                                                                                                                        Regulations could be tightened in the EU by including additional commodities under regulatory control, clearly prescribing the inspection procedures and the appropriate treatments to be used, and combining these with other measures, such as screening (EFSA, 2012). The application of protected zones to areas where L. trifolii is not yet present could help prevent further spread of the pest.

                                                                                                                                                                                                                        A phytosanitary certificate should be required for cut flowers and for vegetables with leaves. 

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                                                                                                                                                                                                                        Distribution References

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                                                                                                                                                                                                                        Links to Websites

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                                                                                                                                                                                                                        GISD/IASPMR: Invasive Alien Species Pathway Management Resource and DAISIE European Invasive Alien Species Gatewayhttps://doi.org/10.5061/dryad.m93f6Data source for updated system data added to species habitat list.
                                                                                                                                                                                                                        Global register of Introduced and Invasive species (GRIIS)http://griis.org/Data source for updated system data added to species habitat list.

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