Invasive Species Compendium

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Datasheet

Tuta absoluta
(South American tomato pinworm)

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Datasheet

Tuta absoluta (South American tomato pinworm)

Summary

  • Last modified
  • 12 February 2021
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Natural Enemy
  • Preferred Scientific Name
  • Tuta absoluta
  • Preferred Common Name
  • South American tomato pinworm
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Arthropoda
  •       Subphylum: Uniramia
  •         Class: Insecta
  • Summary of Invasiveness
  • Tuta absoluta is a major destructive pest of tomato worldwide. There is increasing concern about the rapid geographical expansion of the pest in tomato-growing areas due to the intensification of trade and human movement. T. absoluta...

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Pictures

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PictureTitleCaptionCopyright
Tuta absoluta  (tomato leafminer); larval damage on tomato (Lycopersicon esculentum).
TitleLarval damage
CaptionTuta absoluta (tomato leafminer); larval damage on tomato (Lycopersicon esculentum).
Copyright©Marja van der Straten Organization/NVWA Plant Protection Service/Bugwood - CC BY-NC 3.0 US
Tuta absoluta  (tomato leafminer); larval damage on tomato (Lycopersicon esculentum).
Larval damageTuta absoluta (tomato leafminer); larval damage on tomato (Lycopersicon esculentum).©Marja van der Straten Organization/NVWA Plant Protection Service/Bugwood - CC BY-NC 3.0 US
Tuta absoluta (tomato leafminer); adult at rest.
TitleAdult
CaptionTuta absoluta (tomato leafminer); adult at rest.
Copyright©Marja van der Straten Organization/NVWA Plant Protection Service/Bugwood - CC BY-NC 3.0 US
Tuta absoluta (tomato leafminer); adult at rest.
AdultTuta absoluta (tomato leafminer); adult at rest.©Marja van der Straten Organization/NVWA Plant Protection Service/Bugwood - CC BY-NC 3.0 US
Tuta absoluta (tomato leafminer); adult male. Museum set specimen. (Note scale)
TitleAdult
CaptionTuta absoluta (tomato leafminer); adult male. Museum set specimen. (Note scale)
Copyright©Sangmi Lee/Hasbrouck Insect Collection, Arizona State University/Bugwood.org - CC BY 3.0 US
Tuta absoluta (tomato leafminer); adult male. Museum set specimen. (Note scale)
AdultTuta absoluta (tomato leafminer); adult male. Museum set specimen. (Note scale)©Sangmi Lee/Hasbrouck Insect Collection, Arizona State University/Bugwood.org - CC BY 3.0 US
Tuta absoluta (tomato leafminer); single egg on a tomato leaf.
TitleEgg
CaptionTuta absoluta (tomato leafminer); single egg on a tomato leaf.
Copyright©M.A. Uchoa-Fernandes
Tuta absoluta (tomato leafminer); single egg on a tomato leaf.
EggTuta absoluta (tomato leafminer); single egg on a tomato leaf.©M.A. Uchoa-Fernandes
Tuta absoluta (tomato leafminer); pupae - 1) male.  2) female.
TitlePupae
CaptionTuta absoluta (tomato leafminer); pupae - 1) male. 2) female.
Copyright©M.A. Uchoa-Fernandes
Tuta absoluta (tomato leafminer); pupae - 1) male.  2) female.
PupaeTuta absoluta (tomato leafminer); pupae - 1) male. 2) female.©M.A. Uchoa-Fernandes
Tuta absoluta (tomato leafminer); pupa, close to emergence of adult moth.
TitlePupa
CaptionTuta absoluta (tomato leafminer); pupa, close to emergence of adult moth.
Copyright©M.A. Uchoa-Fernandes
Tuta absoluta (tomato leafminer); pupa, close to emergence of adult moth.
PupaTuta absoluta (tomato leafminer); pupa, close to emergence of adult moth.©M.A. Uchoa-Fernandes
Tuta absoluta (tomato leafminer); natural enmy. Adult of Spilochalcis sp. (Hymeoptera, Chalcididae), a pupal parasite of T. absoluta, native to Brazil.
TitleNatural enemy
CaptionTuta absoluta (tomato leafminer); natural enmy. Adult of Spilochalcis sp. (Hymeoptera, Chalcididae), a pupal parasite of T. absoluta, native to Brazil.
Copyright©M.A. Uchoa-Fernandes
Tuta absoluta (tomato leafminer); natural enmy. Adult of Spilochalcis sp. (Hymeoptera, Chalcididae), a pupal parasite of T. absoluta, native to Brazil.
Natural enemyTuta absoluta (tomato leafminer); natural enmy. Adult of Spilochalcis sp. (Hymeoptera, Chalcididae), a pupal parasite of T. absoluta, native to Brazil.©M.A. Uchoa-Fernandes
Macrolophus pygmaeus; a true bug (Heteroptera: Miridae) and a potentially useful biocontrol against the tomato leafminer (Tuta absoluta). This specimen is from Lohja, Finland. June 2017.
TitleNatural enemy
CaptionMacrolophus pygmaeus; a true bug (Heteroptera: Miridae) and a potentially useful biocontrol against the tomato leafminer (Tuta absoluta). This specimen is from Lohja, Finland. June 2017.
Copyright©Petro Pynnönen/via wikipedia - CC BY-SA 4.0
Macrolophus pygmaeus; a true bug (Heteroptera: Miridae) and a potentially useful biocontrol against the tomato leafminer (Tuta absoluta). This specimen is from Lohja, Finland. June 2017.
Natural enemyMacrolophus pygmaeus; a true bug (Heteroptera: Miridae) and a potentially useful biocontrol against the tomato leafminer (Tuta absoluta). This specimen is from Lohja, Finland. June 2017.©Petro Pynnönen/via wikipedia - CC BY-SA 4.0

Identity

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Preferred Scientific Name

  • Tuta absoluta (Meyrick)

Preferred Common Name

  • South American tomato pinworm

Other Scientific Names

  • Gnorimoschema absoluta (Meyrick, 1917) Clarke, 1962
  • Phthorimaea absoluta (Meyrick, 1917)
  • Scrobipalpula absoluta (Meyrick, 1917) Povolny, 1964
  • Scrobipalpuloides absoluta (Meyrick, 1917) Povolny, 1987

International Common Names

  • English: South American tomato moth; tomato leafminer
  • Spanish: cogollero del tomate; gusano minador del tomate; minador de hojas y tallos de la papa; oruga minadora de hoja y tallo; polilla del tomate; polilla perforadora del tomate
  • French: mineuse de la tomate; mineuse sud-américaine de la tomate
  • Russian: южноамериканская томатная моль
  • Chinese: 南美番茄潜叶蛾; 番茄潛旋蛾
  • Portuguese: traça-do-tomateiro

Local Common Names

  • Denmark: tomatmøl
  • Italy: tignola del pomodoro
  • Netherlands: tomatenmineermot
  • Norway: sør-amerikansk tomatmøll; tomatmøll
  • Sweden: tomatmal

EPPO code

  • GNORAB (Tuta absoluta)

Summary of Invasiveness

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Tuta absoluta is a major destructive pest of tomato worldwide. There is increasing concern about the rapid geographical expansion of the pest in tomato-growing areas due to the intensification of trade and human movement. T. absoluta was first collected in Huancayo, Peru in 1917. Between the mid-1960s and the 1990s, it spread to all South American countries. It was observed for the first time outside of South America, in eastern Spain in 2006, and within a few years, had spread into most countries of the Mediterranean basin. Currently, it can be found throughout Europe, the Middle East, Africa and parts of Asia. Upon reaching the northern coast of Africa and the sub-Saharan region, the pest started moving swiftly southwards reaching the Republic of Benin in 2017 and Togo in 2018. Despite efforts to prevent T. absoluta invasion in China, the pest arrived there in 2017. T. absoluta is still spreading on the American continent, and its presence in Costa Rica was reported in 2014, increasing quarantine concern and the need for further information on dispersion dynamics and sustainable management options in Central and North America (USA and Canada).

T. absoluta has quickly reached economic pest status on tomato in invaded areas despite the efforts of plant protection agencies.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Arthropoda
  •             Subphylum: Uniramia
  •                 Class: Insecta
  •                     Order: Lepidoptera
  •                         Family: Gelechiidae
  •                             Genus: Tuta
  •                                 Species: Tuta absoluta

Notes on Taxonomy and Nomenclature

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Tuta absoluta was originally described as Phthorimaea absoluta by Meyrick in 1917. The description was based on a male specimen collected in Huancayo, Peru (Meyrick, 1917). This specimen is deposited in the Natural History Museum, London, UK.

The genus of this species has been changed three times: Clarke (1962) changed the genus to Gnorimoschema Busck 1900. In 1967, Povolny, applying morphological characters based on its genitalia, placed the species in the genus Scrobipalpula Povolny 1964. After revision of the Gnorimoschenini (Gelechiinae), the genus Scrobipalpuloides was erected to place absoluta (Povolny, 1987). The current scientific name of the species is Tuta absoluta (Meyrick 1917) (Povolny, 1994). As other Gelechiidae moths are easily confused with this species, accurate identification of T. absoluta can be accomplished by using male genitalia characters or DNA barcoding methods (Zhang et al., 2013).

Description

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The life-cycle of Tuta absoluta comprises four biological stages: egg, larva (four stages), pupa and adult. The larval stage is responsible for causing damage on several plant parts. After eclosion of the eggs, the first-stage larvae penetrates the leaves, stems or fruits to develop inside (Abbes et al., 2012b).

Egg

Females lay the eggs individually on the underside of leaves, stems and sepals. The eggs are elliptical, and their colour varies from oyster-white to bright yellow, darkening in the embryonic phase and becoming brown prior to eclosion (Imenes et al., 1990).

Larva

The first-instar larvae are whitish soon after egg eclosion, becoming greenish after feeding on plants. In the second and third instars the colour changes to light pink according to the food ingested (i.e., leaflet or ripe fruit). Fourth-instar larvae have a patterned prothoracic shield and a pink colour on the back (Abbes et al., 2012b).

Prepupa and pupa

The prepupae are lighter green than the feeding larvae (first to fourth instars) and develop a distinguishing pink coloration on the dorsal surface. They leave the mines and build silk cocoons on the leaflets or in the soil, according to the habitat chosen for pupation. When pupation occurs inside mines or fruit, the prepupae do not build cocoons.

Pupae are obtecta, 5 mm long, with a greenish coloration at first, turning chestnut brown and dark brown near-adult emergence (Imenes et al., 1990).

Adult

Adult moths are about 10 mm long, and covered by silverfish-grey scales. The antennae have a filiform shape, alternating between light or dark segments, and their mouthparts are comprised of recurved labial palps, which are well developed (Imenes et al., 1990).

Distribution

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T. absoluta was observed for the first time outside of South America, in eastern Spain, in 2006. Currently, it can be found throughout Europe, Africa, the Middle East, and parts of Asia (Desneux et al., 2010; Campos et al., 2017; Biondi et al., 2018; Mansour et al., 2018).

Upon reaching the northern coast of Africa and the sub-Saharan region, the pest started moving swiftly southwards and has now invaded most of Africa (Mansour et al., 2018). This was due to the spatial continuity of vegetable cultivation across political borders as well as the absence of effective surveillance mechanisms, ever-growing tourism, and increasing intra-continental trade (Sylla et al., 2017).

Despite efforts to prevent invasion, T. absoluta was first detected in China in 2017 (Zhang et al., 2020). The risk of introduction into China had increased considerably due to infestations in bordering countries with a high risk of T. absoluta outbreaks, such as Tajikistan (Saidov et al., 2018) and Kyrgyzstan (Uulu et al., 2017).

T. absoluta is still spreading on the American continent, and its presence in Costa Rica was reported in 2014, increasing quarantine concern and the need for further information on dispersion dynamics and sustainable management options in Central and North America (USA, Mexico and Canada) (Campos et al., 2017).

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

AlgeriaPresent, LocalizedIntroduced2008
AngolaPresentIntroduced
BeninPresentIntroduced2017
BotswanaPresent
Burkina FasoPresentIntroduced2016
BurundiPresentIntroducedvia PestLens newsletter.
Cabo VerdePresent
CameroonPresentIntroduced
Congo, Democratic Republic of thePresent
Côte d'IvoirePresent
EgyptPresent, WidespreadIntroduced2009
Equatorial GuineaPresent
EthiopiaPresent
GhanaPresent, LocalizedIntroduced
KenyaPresent
LesothoPresent, Transient under surveillanceIntroduced2018Present: only in some areas
LibyaPresent, LocalizedIntroduced2009
MalawiPresentIntroduced
MayottePresent, Widespread
MoroccoPresent, WidespreadIntroduced2008
MozambiquePresent, WidespreadIntroduced2017
NamibiaPresent
NigerPresent, Localized
NigeriaPresent
RwandaPresent, LocalizedIntroduced2015
São Tomé and PríncipePresent
SenegalPresentIntroduced2013
SeychellesPresentIntroduced
South AfricaPresent, Localized
SudanPresent, LocalizedIntroduced2010
TanzaniaPresent, LocalizedIntroduced2014
TogoPresentIntroduced2018
TunisiaPresent, WidespreadIntroduced2008
UgandaPresent, Widespread
ZambiaPresent, Widespread
ZimbabwePresent

Asia

AfghanistanPresentIntroduced
ArmeniaPresent, Few occurrences
AzerbaijanPresent
BahrainAbsent, Unconfirmed presence record(s)
BangladeshPresentIntroduced2016via PestLens newsletter.
ChinaPresent, LocalizedIntroduced2017Invasive
-XinjiangPresent, Localized
GeorgiaPresent
IndiaPresent, LocalizedIntroduced2014
-Andhra PradeshPresent
-ChhattisgarhPresentIntroducedFirst reported: 2015-16
-DelhiPresent
-GujaratPresent
-HaryanaPresent
-Himachal PradeshPresent
-KarnatakaPresentIntroduced2014
-KeralaPresent
-Madhya PradeshPresentIntroduced2017
-MaharashtraPresentIntroduced2014
-MeghalayaPresentIntroduced
-PunjabPresentIntroducedFirst reported: 2016-17
-Tamil NaduPresentIntroduced
-TelanganaPresent
-Uttar PradeshPresent
-UttarakhandPresentIntroduced
IranPresentIntroduced2010
IraqPresent, Localized
IsraelPresentIntroduced2009
JapanAbsent, Unconfirmed presence record(s)
JordanPresent, WidespreadIntroduced2009
KazakhstanPresent, Localized
KuwaitAbsent, Unconfirmed presence record(s)
KyrgyzstanPresent, Localized
LebanonAbsent, Unconfirmed presence record(s)
MyanmarPresent
NepalPresent, Localized
PakistanPresentIntroduced2020
QatarPresent, Few occurrencesIntroduced2011
Saudi ArabiaPresent, Localized
SyriaPresent, LocalizedIntroduced2010
TajikistanPresent, Localized
TurkeyPresent, LocalizedIntroduced2009
TurkmenistanPresentIntroduced2015
United Arab EmiratesPresent, LocalizedIntroduced2012
UzbekistanPresentIntroduced2016
YemenPresent, LocalizedIntroduced2013

Europe

AlbaniaPresent, LocalizedIntroduced2009
AustriaPresent, Localized
BelarusAbsent, Eradicated
BelgiumPresent, LocalizedIntroduced2009
Bosnia and HerzegovinaPresent, Localized
BulgariaPresent, LocalizedIntroduced2009
CroatiaPresent, LocalizedIntroduced2010
CyprusPresent, WidespreadIntroduced2009
CzechiaPresent, Widespread
DenmarkAbsent, Intercepted only
FrancePresent, LocalizedIntroduced2009
-CorsicaPresent, Few occurrences
GermanyPresent, Transient under eradication
GreecePresent, LocalizedIntroduced2009
-CretePresent, LocalizedIntroduced
GuernseyPresent, Few occurrences
HungaryPresent, Localized
ItalyPresent, WidespreadIntroduced2008
-SardiniaPresent, WidespreadIntroduced
-SicilyPresentIntroduced
LithuaniaPresent, Few occurrencesIntroduced2009
MaltaPresent, Localized
MoldovaPresent
MontenegroPresent, WidespreadIntroduced2010
NetherlandsPresent
North MacedoniaPresent
NorwayPresent, Localized
PortugalPresent, Localized
-AzoresPresentIntroduced
RomaniaPresentIntroduced2009
RussiaPresent, Localized
-Southern RussiaPresent, LocalizedIntroduced
SerbiaPresent, LocalizedIntroduced2011
Serbia and MontenegroPresent, Few occurrences
SlovakiaPresent, Few occurrences
SloveniaPresent, LocalizedIntroduced
SpainPresent, WidespreadIntroduced2006
-Balearic IslandsPresent, Localized
-Canary IslandsPresent
SwitzerlandPresent, Localized
UkrainePresent, Transient under eradication
United KingdomPresent, LocalizedIntroduced2009
-Channel IslandsPresentIntroduced
-EnglandPresent, Localized

North America

Costa RicaPresent, WidespreadIntroduced2014
HaitiPresentIntroduced2018via PestLens newsletter.
PanamaPresent, Localized

South America

ArgentinaPresent, WidespreadIntroduced1964
BoliviaPresent, WidespreadIntroduced1983
BrazilPresent, WidespreadIntroduced1979
-BahiaPresent
-CearaPresent
-Distrito FederalPresent
-Espirito SantoPresent
-GoiasPresent
-Mato GrossoPresent
-Minas GeraisPresent
-ParanaPresent
-PernambucoPresent
-Rio de JaneiroPresent
-Rio Grande do SulPresent
-Santa CatarinaPresent
-Sao PauloPresent
ChilePresent, Widespread
-Easter IslandPresent
ColombiaPresent, WidespreadIntroduced1989
EcuadorPresentIntroduced1989
ParaguayPresentIntroduced1994
PeruPresent, Widespread
UruguayPresentIntroduced1995
VenezuelaPresent, WidespreadIntroduced1964

History of Introduction and Spread

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From the mid-1960s to the mid-1990s T. absoluta spread throughout the South American continent reaching Brazil, the main tomato producer in the region, in the early 1980s (Guedes and Picanço, 2012). Between the 1980s and late-2000s, T. absoluta became the main pest of tomato in the region, notoriously difficult to control (Guedes and Picanço 2012; Biondi et al., 2018). T. absoluta was observed for the first time outside of South America, in eastern Spain, in 2006. It can now be found throughout Europe, Africa, the Middle East, and parts of Asia (Desneux et al., 2010; Campos et al., 2017; Biondi et al., 2018). The African continent has been almost totally invaded since the detection of the pest in Morocco in 2008. Upon reaching the northern coast of Africa and the sub-Saharan region, T. absoluta started moving swiftly southwards (Sylla et al., 2017; Mansour et al., 2018). This spread was due to the spatial continuity of vegetable cultivation across political borders, the absence of effective surveillance mechanisms, the lack of specific phytosanitary expertise to intercept infested vegetables, ever-growing tourism, and increasing intra-continental trade (Sylla et al., 2017). T. absoluta was reported in Turkey in 2009 (Seplyarsky et al., 2010) and since then spread steadily across 15 western Asian countries between 2010 and 2015 (Campos et al., 2017; Han et al., 2019). T. absoluta has recently been reported in several places in southern Asia, including India in 2014 (western India) (Sridhar et al., 2014; Kalleshwaraswamy et al., 2015) and 2017 (northeastern India) (Sankarganesh et al., 2017); Bangladesh (Hossain et al., 2016) and Nepal (Bajracharya et al., 2016) in 2016; central Asia in Kazakhstan (Agroalem, 2016); Turkmenistan in 2015 (Bratu et al., 2015); and Kyrgyzstan in 2017 (Uulu et al., 2017). There were also reports of its suspected occurrence in Pakistan (southern Asia) in 2014, Oman in 2014 and Azerbaijan in 2016 (western Asia), Tajikistan and Uzbekistan in 2016 (Campos et al., 2017), and Myanmar (eastern Asia) in 2017 (Biondi et al., 2018; Han et al., 2019). Despite efforts to prevent the invasion of T. absoluta in China, this pest arrived there in 2017 (Zhang et al., 2020). The risk of introduction into China had increased considerably due to infested countries which border China, such as Tajikistan (Saidov et al., 2018) and Kyrgyzstan (Uulu et al., 2017), being under high risk of T. absoluta outbreaks. T. absoluta is still spreading on the American continent, and was reported in Costa Rica in 2014, increasing quarantine concern in Central and North America (USA, Mexico and Canada).

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Argentina Chile 1964 Crop production (pathway cause) Yes No Bahamondes and Mallea (1969) Pest was accidentally introduced by transporting tomatoes between border regions
Spain Chile 2006 Crop production (pathway cause) Yes No Urbaneja et al. (2007) Pest was accidentally introduced by airfreight transporting tomatoes

Risk of Introduction

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The risk of a global distribution with additional invasion is high, with recent movement northward from South America to Central America, the rapid spread across Asian and African countries, and human-assisted spread through trading routes (McNitt et al., 2019), so that countries such as New Zealand, the USA and Australia may ultimately be invaded (Biondi et al., 2018).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial ManagedCultivated / agricultural land Principal habitat Harmful (pest or invasive)
Terrestrial ManagedProtected agriculture (e.g. glasshouse production) Principal habitat Harmful (pest or invasive)
Terrestrial ManagedDisturbed areas Secondary/tolerated habitat Natural
Terrestrial ManagedUrban / peri-urban areas Secondary/tolerated habitat Natural
TerrestrialTerrestrial ‑ Natural / Semi-natural Secondary/tolerated habitat Natural
Terrestrial Natural / Semi-naturalNatural forests Secondary/tolerated habitat Natural
Terrestrial Natural / Semi-naturalArid regions Secondary/tolerated habitat Natural

Hosts/Species Affected

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T. absoluta is mainly associated with tomato plants (Solanum lycopersicum), but it can oviposit and develop on a wide range of cultivated and wild plant species. Many species of Solanaceae allow T. absoluta feeding, development and reproduction, such as potato (S. tuberosum), aubergine (S. melongena), pepino (S. muricatum) and black nightshade (S. nigrum [S. americanum]) (Cherif et al., 2019). There are references to other hosts in the family Solanaceae (Lycopersicon hirsutum [S. habrochaites], Solanum lyratum and Solanum sp.) (Clarke, 1962; Vargas, 1970; Coelho and França, 1987). Additionally, T. absoluta was able to complete its development on some wild Solanaceae species including Lycopersicum puberulum [Lycopersicon puberulum], Datura ferox, D. stramonium and Nicotiana glauca (Garcia and Espul, 1982). However, in other solanaceous species, the female did not lay eggs, such as Salpichroa origanifolia, D. ferox and Physalis viscosa (Galarza, 1984). In particular, T. absoluta showed the ability to overwinter, yet at low population density, on winter potato and black nightshade (Cocco et al., 2015). Therefore, alternative hosts in winter may represent a source of re-infestation for spring-summer tomato crops.

Studies have highlighted plants belonging to Amaranthaceae, Cucurbitaceae, Fabaceae, Euphorbiaceae, Malvaceae and Asteraceae, which are reported as alternative hosts for this pest. Convolvulaceae are not suitable alternative hosts for T. absoluta: no oviposition was observed on Calystegia sepium and Convolvulus arvensis. In addition, T. absoluta does not oviposit on Beta vulgaris and Chenopodium album (Amaranthaceae) (Bawin et al., 2016). T. absoluta could not develop on other plant species such as Geranium robertianum (Geraniaceae) and Cucurbita pepo (Cucurbitaceae) (Ingegno et al., 2017).

Host Plants and Other Plants Affected

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Plant nameFamilyContextReferences
Solanum chenopodioidesSolanaceaeUnknown
Amaranthus spinosus (spiny amaranth)AmaranthaceaeUnknown
Amaranthus viridis (slender amaranth)AmaranthaceaeOther
    Atropa belladonna (deadly nightshade)SolanaceaeUnknown
    Beta vulgaris (beetroot)ChenopodiaceaeOther
      Capsicum (peppers)SolanaceaeOther
        Capsicum annuum (bell pepper)SolanaceaeMain
        Chenopodium album (fat hen)ChenopodiaceaeUnknown
        Chenopodium bonus-henricusChenopodiaceaeWild host
          Chenopodium rubrumChenopodiaceaeWild host
            Citrullus lanatus (watermelon)CucurbitaceaeUnknown
            Convolvulus arvensis (bindweed)ConvolvulaceaeWild host
            Cucumis sativus (cucumber)CucurbitaceaeUnknown
            Datura stramonium (jimsonweed)SolanaceaeWild host
            Jatropha curcas (jatropha)EuphorbiaceaeUnknown
            Lycium barbarum (Matrimonyvine)SolanaceaeUnknown
            Lycopersicon pennelliiSolanaceaeUnknown
            Lycopersicon pimpinellifolium (currant tomato)SolanaceaeUnknown
            Medicago sativa (lucerne)FabaceaeUnknown
            Nicotiana glauca (tree tobacco)SolanaceaeWild host
            Nicotiana rustica (wild tobacco)SolanaceaeUnknown
            Nicotiana tabacum (tobacco)SolanaceaeUnknown
            Phaseolus vulgaris (common bean)FabaceaeUnknown
            • Ðurić et al. (2016)
            Physalis angulata (cutleaf groundcherry)SolanaceaeOther
            Physalis peruviana (Cape gooseberry)SolanaceaeUnknown
            Piper nigrum (black pepper)PiperaceaeUnknown
            Salpichroa origanifoliaSolanaceaeUnknown
            Sinapis arvensis (wild mustard)BrassicaceaeUnknown
              Solanum (nightshade)SolanaceaeUnknown
              Solanum americanumSolanaceaeUnknown
              Solanum bonarienseSolanaceaeUnknown
              Solanum cheesmaniaeSolanaceaeUnknown
              Solanum dubiumSolanaceaeWild host
              Solanum dulcamara (bittersweet nightshade)SolanaceaeUnknown
              Solanum elaeagnifolium (silverleaf nightshade)SolanaceaeUnknown
              Solanum galapagenseUnknown
              Solanum habrochaitesSolanaceaeUnknown
              Solanum lycopersicum (tomato)SolanaceaeMain
              Solanum melongena (aubergine)SolanaceaeOther
              Solanum muricatum (melon pear)SolanaceaeOther
              Solanum nigrum (black nightshade)SolanaceaeWild host
                Solanum pennelliiUnknown
                Solanum pseudocapsicum (Jerusalem-cherry)SolanaceaeUnknown
                Solanum sisymbriifolium (sticky nightshade)SolanaceaeUnknown
                Solanum tuberosum (potato)SolanaceaeOther
                Solanum woronowiiSolanaceaeOther
                Sonchus oleraceus (common sowthistle)AsteraceaeWild host
                  Sorghum halepense (Johnson grass)PoaceaeOther
                  Spinacia oleracea (spinach)ChenopodiaceaeOther
                    Xanthium strumarium (common cocklebur)AsteraceaeOther

                    Growth Stages

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                    Flowering stage, Fruiting stage, Post-harvest, Seedling stage, Vegetative growing stage

                    List of Symptoms/Signs

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                    SignLife StagesType
                    Fruit / abnormal shape
                    Fruit / frass visible
                    Fruit / internal feeding
                    Fruit / obvious exit hole
                    Fruit / premature drop
                    Fruit / reduced size
                    Growing point / dead heart
                    Growing point / distortion
                    Growing point / frass visible
                    Growing point / internal feeding; boring
                    Growing point / lesions
                    Inflorescence / external feeding
                    Inflorescence / fall or shedding
                    Inflorescence / frass visible
                    Inflorescence / internal feeding
                    Leaves / abnormal forms
                    Leaves / external feeding
                    Leaves / frass visible
                    Leaves / internal feeding
                    Leaves / leaves rolled or folded
                    Leaves / necrotic areas
                    Stems / dead heart
                    Stems / dieback
                    Stems / distortion
                    Stems / internal feeding
                    Stems / visible frass
                    Stems / wilt
                    Stems / witches broom
                    Whole plant / dead heart
                    Whole plant / distortion; rosetting
                    Whole plant / frass visible
                    Whole plant / internal feeding
                    Whole plant / plant dead; dieback

                    Biology and Ecology

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                    T. absoluta presents multivoltine behaviour, which allows its population to increase very quickly (Desneux et al., 2010; Garzia et al., 2012). The optimum temperature for T. absoluta to develop is 30°C (rm = 0.12), and the upper and lower temperature thresholds were estimated to be 34.6 and 14°C, respectively (Martins et al., 2016). T. absoluta presents cold tolerance at 0°C in every developmental stage. However, the ability to develop or reproduce at low temperatures has not been reported.

                    Females of T. absoluta lays an average of 260 eggs during their lifetime. The peak of oviposition occurs in the first and second days after adult mating when around 92% of the eggs are laid. The eclosion of eggs occurs at about 5-7 days at 26-30°C and 60-75% relative humidity. Under these conditions, the larvae pass through four instars, which are completed in around 20 days. The larvae mine the mesophyll of the leaf to feed. At high densities, axillary buds of young stems and/or tomato fruits are also damaged (Desneux et al., 2010). After this period, the larva eliminates all material in the gut, and drops to the soil to build a cocoon for pupation. Pupation lasts about 9-12 days for females and 10-13 days for males. Females often emerge from their pupae before the males. Under laboratory conditions, the adults will live for 18-28 days (Rostami et al., 2017). T. absoluta has differentiated behaviour in pupation when it occurs in processing tomato or fresh market tomato plants. In processing tomato, it pupates in the soil (1-2 cm deep) and in fresh market tomato plants, the larvae build a cocoon and pupate on the leaf surface or inside mines (Uchoa-Fernandes et al., 1995b). Pupation is usually higher on leaves, followed by the soil, main stems and fruit (Torres et al., 2001).

                    Females use plant volatiles for orientation toward their hosts, thus contact with plants induces oviposition (Proffit et al., 2011). The female releases a potent sex pheromone on the first or second day after emergence that lures males to exhibit mating behaviour and copulation. The average number of matings for a female in the laboratory was about 10.4, and this behaviour could range from a few minutes up to 6 hours (Imenes et al., 1990; Uchoa-Fernandes et al., 1995a; Lee et al., 2014). The males and females are sexually active from the first day of emergence. They present crepuscular and polygamous behaviour (Biondi et al., 2018). The sex pheromone of T. absoluta has been isolated and identified. The main compounds are tetradecatrienyl acetate and tetradecadienyl acetate in the proportions of 91:9, respectively (Attygalle et al., 1995; Uchoa-Fernandes et al., 1995a).

                    Climate

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                    ClimateStatusDescriptionRemark
                    A - Tropical/Megathermal climate Preferred Average temp. of coolest month > 18°C, > 1500mm precipitation annually
                    Af - Tropical rainforest climate Preferred > 60mm precipitation per month
                    Am - Tropical monsoon climate Preferred Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))
                    As - Tropical savanna climate with dry summer Preferred < 60mm precipitation driest month (in summer) and < (100 - [total annual precipitation{mm}/25])
                    Aw - Tropical wet and dry savanna climate Preferred < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])
                    B - Dry (arid and semi-arid) Tolerated < 860mm precipitation annually
                    BS - Steppe climate Tolerated > 430mm and < 860mm annual precipitation
                    BW - Desert climate Tolerated < 430mm annual precipitation
                    C - Temperate/Mesothermal climate Preferred Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C
                    Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
                    Cw - Warm temperate climate with dry winter Preferred Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)
                    Cf - Warm temperate climate, wet all year Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
                    D - Continental/Microthermal climate Tolerated Continental/Microthermal climate (Average temp. of coldest month < 0°C, mean warmest month > 10°C)
                    Ds - Continental climate with dry summer Tolerated Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)
                    Dw - Continental climate with dry winter Tolerated Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)
                    Df - Continental climate, wet all year Tolerated Continental climate, wet all year (Warm average temp. > 10°C, coldest month < 0°C, wet all year)

                    Latitude/Altitude Ranges

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                    Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
                    44 35

                    Air Temperature

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                    Parameter Lower limit Upper limit
                    Absolute minimum temperature (ºC) 3
                    Mean annual temperature (ºC) 12 30
                    Mean maximum temperature of hottest month (ºC) 30 35
                    Mean minimum temperature of coldest month (ºC) 3 7

                    Rainfall

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                    ParameterLower limitUpper limitDescription
                    Dry season duration3 mm4 mmnumber of consecutive months with <40 mm rainfall
                    Mean annual rainfall280 mm1500 mmmm; lower/upper limits

                    Rainfall Regime

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                    Summer
                    Uniform

                    Natural enemies

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                    Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
                    Agathis fuscipennis Parasite Arthropods|Larvae Loni et al. (2011)
                    Apanteles gelechiidivoris Parasite Arthropods|Larvae Bajonero et al. (2008) Chile
                    Bacillus thuringiensis Pathogen Giustolin et al. (2001)
                    Bacillus thuringiensis kurstaki Pathogen Arthropods|Larvae Giustolin et al. (2001)
                    Bacillus thuringiensis thuringiensis Pathogen Arthropods|Larvae
                    Beauveria bassiana Pathogen Pires et al. (2009)
                    Bracon Parasite Marchiori et al. (2004)
                    Bracon lucileae Parasite Arthropods|Larvae Desneux et al. (2010)
                    Copidosoma Parasite Eggs Desneux et al. (2010)
                    Copidosoma koehleri Parasite Eggs Gervassio et al. (2019)
                    Diadegma Parasite Arthropods|Pupae Zappalà et al. (2012)
                    Dicladocerus Parasite Arthropods|Larvae
                    Dicyphus errans Predator Ingegno et al. (2013)
                    Dineulophus phthorimaeae Parasite Luna et al. (2015)
                    Dolichogenidea gelechiidivoris Parasite Aigbedion-Atalor et al. (2020)
                    Earinus Parasite Marchiori et al. (2004)
                    Elachertus inunctus Parasite Yarahmadi et al. (2016)
                    Elachertus pulcher Parasite Yarahmadi et al. (2016)
                    Engytatus varians Predator Eggs; Arthropods|Larvae Pérez-Aguilar et al. (2018)
                    Granulosis virus Pathogen Gómez Valderrama et al. (2018)
                    Haltichella Parasite Arthropods|Pupae McCravy et al. (2001)
                    Horismenus Parasite Arthropods|Larvae Desneux et al. (2010)
                    Macrolophus basicornis Predator Eggs; Arthropods|Pupae Soares et al. (2019)
                    Macrolophus pygmaeus Predator Urbaneja et al. (2009)
                    Metarhizium anisopliae Pathogen Pires et al. (2009)
                    Nabis pseudoferus Predator Arthropods|Larvae Mahdavi et al. (2020)
                    Necremnus tutae Parasite Arthropods|Larvae Gebiola et al. (2015)
                    Neochrysocharis formosa Parasite Guleria et al. (2020)
                    Nesidiocoris tenuis Predator El-Arnaouty and Kortam (2012)
                    Parasierola nigrifemur Parasite Arthropods|Larvae
                    Spilochalcis Parasite Arthropods|Pupae Desneux et al. (2010)
                    Steinernema carpocapsae Parasite Batalla-Carrera et al. (2010)
                    Steinernema feltiae Parasite Arthropods|Larvae Batalla-Carrera et al. (2010)
                    Stenomesius japonicus Parasite Arthropods|Larvae Gabarra et al. (2014)
                    Tetrastichus Parasite Arthropods|Larvae Desneux et al. (2010)
                    Trichogramma exiguum Parasite Eggs Desneux et al. (2010)
                    Trichogramma nerudai Parasite Querino and Zucchi (2003)
                    Trichogramma pretiosum Parasite Eggs Cônsoli et al. (1998)
                    Tupiocoris cucurbitaceus Predator Eggs Cagnotti et al. (2020)

                    Notes on Natural Enemies

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                    Multiple parasitoids have been identified parasitizing T. absoluta in South America and in newly invaded regions. Egg parasitoids, notably species of Trichogramma are found controlling T. absoluta through inundative releases. Several species, notably T. pretiosum, T. acheae and T. euproctidis, proved technically viable as biocontrol agents (up to 90% parasitism) in tomato greenhouses in Brazil, Spain and Egypt, respectively (Uchoa-Fernandes and Campos, 1993; Zappalà et al., 2013; El-Arnaouty et al., 2014).

                    Larval parasitoids have been documented against T. absoluta. The main species studied as potential biological control agents are Pseudapanteles dignus and Dineulophus phthorimaeae, with up to 40% parasitism in South America, and Bracon nigricans, Stenomesius japonicus and Necremnus tutae in Europe (Ferracini et al., 2012; Biondi et al., 2013; Chailleux et al., 2017).

                    Hemipteran predators, notably anthocorids, geocorids, mirids, nabids and pentatomids, have been identified as effective predators against T. absoluta in both native and invaded areas. The mirids Nesidiocoris tenuis and Macrolophus pygmaeus occur spontaneously in most Mediterranean countries, but also are commercially available (Biondi et al., 2018).

                    Microbial control has been evaluated and relies mostly on commercial strains of Bacillus thuringiensis var. kurstaki and aizawaii (González-Cabrera et al., 2011). Additionally, studies with the fungi Beauveria bassiana and Metarhizium anisopliae have been developed but have still not resulted in commercial products specifically designed for T. absoluta (Pires et al., 2009, 2010).

                    Nematodes (Steinernema and Heterorhabditis spp.) also considerably reduce plant infestation by T. absoluta under laboratory and greenhouse conditions, though there has been no reported use in commercial greenhouses or in the open field (Batalla-Carrera et al., 2010).

                    Biological control programmes against T. absoluta should rely on the combined use of complementary biocontrol agents such as parasitoids, microbials and/or mirid predators to maximize biocontrol (Mansour and Biondi, 2020).

                    Means of Movement and Dispersal

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                    Natural Dispersal

                    In the invaded areas, the spread is mainly happening by natural means. Wind currents seem to be especially favourable for its dispersal, though the real flight capacity of adults remains

                    uncertain (Desneux et al., 2010). The recent and fast invasion history in Europe, Africa and the Middle East implies that areas with large monocultures of tomato and other host crops favour the natural expansion of T. absoluta (Biondi et al., 2018).

                    Accidental Introduction

                    The key pathway for the long-distance spread among countries and continents is primarily accidental introduction by agricultural trade, mostly by tomato fruits, but tomato seedlings and other host plants may also be involved. The spread of T. absoluta in South America has been attributed to the tomato fruit trade and this hypothesis is supported by the interceptions of T. absoluta at packaging sites of imported fruits in various countries (Desneux et al., 2011). Molecular studies showed that the invasion in Europe was due to a single introduction of Chile to Spain, probable an infected fruit arrived by airfreight (Guillemaud et al., 2015). In addition, tomato plants grown in greenhouses and plant nurseries may help T. absoluta build up populations upon arrival and survive unfavourable climatic conditions. These sites may possibly as bridgeheads for further invasions (Biondi et al., 2018).

                    Pathway Causes

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                    CauseNotesLong DistanceLocalReferences
                    Crop productionLong-distance: T. absoluta was accidentally introduced by airfreight transporting tomatoes from Chile to Spain. Local: In the northern coast of Africa and the sub-Saharan region, T. absoluta spread southwards due to the high number of plantations of tomato and other solanaceous species. Yes Yes Guillemaud et al. (2015); Sylla et al. (2017)
                    Food Yes
                    HorticultureSouth America, Europe, Africa and Asia Yes Yes Sylla et al. (2017); Campos et al. (2017)

                    Pathway Vectors

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                    VectorNotesLong DistanceLocalReferences
                    AircraftTuta absoluta was accidentally introduced by airfreight transport of fresh fruit tomato from Chile to Spain Yes Guillemaud et al. (2015)
                    Plants or parts of plantsSouth America, Europe, Africa and Asia Yes Yes

                    Plant Trade

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                    Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
                    Flowers/Inflorescences/Cones/Calyx adults; eggs; larvae; pupae Yes Pest or symptoms usually visible to the naked eye
                    Fruits (inc. pods) adults; eggs; larvae; pupae Yes Yes Pest or symptoms usually visible to the naked eye
                    Growing medium accompanying plants adults; eggs; larvae; pupae Yes Pest or symptoms usually visible to the naked eye
                    Leaves adults; eggs; larvae; pupae Yes Yes Pest or symptoms usually visible to the naked eye
                    Seedlings/Micropropagated plants adults; eggs; larvae; pupae Yes Pest or symptoms usually visible to the naked eye
                    Stems (above ground)/Shoots/Trunks/Branches adults; eggs; larvae; pupae Yes 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
                    Roots
                    True seeds (inc. grain)
                    Wood

                    Impact Summary

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                    CategoryImpact
                    Cultural/amenity Negative
                    Economic/livelihood Negative
                    Environment (generally) Negative
                    Human health Negative

                    Economic Impact

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                    T. absoluta poses a major threat to tomato production, and relatively less to potato, aubergine and other solanaceous plant species (Biondi et al., 2018). The economic impact of T. absoluta is directly reflected in the rising costs of tomato crop production, namely additional costs for pest management, a decrease of marketable products, and the potential loss of trading partners through restrictions on export to non-infested countries.

                    In the absence of control measures, T. absoluta can cause up to 80-100% yield losses in tomato crops. It may pose a threat to both greenhouse and open-field tomato production (Guedes et al., 2019). The immediate threat to tomato production in South America led to intensive insecticide use against this pest in invaded areas. When T. absoluta was first observed in Brazil, farmers were applying insecticides 10-12 times per cultivation cycle. After a few years, this number increased to more than 30 applications per cropping cycle, i.e. 4-6 weekly sprays (Guedes and Siqueira, 2012). Consequently, the increased number of insecticide applications against T. absoluta raised tomato production costs.

                    The high reduction of tomato production is mainly due to the severity of T. absoluta attacks, the larvae can bore through the stems, thus killing young plants which in turn compromises yield, or occasionally feed on fruits, increasing the costs for postharvest selection (Galdino et al., 2015). Moreover, indirect damage can also be caused by secondary infections, with pathogens developing on the infested plant and fruit tissues (Garzia et al., 2012). As observed in many countries, it is very difficult to control and limit the spread of T. absoluta. The economic impact based on crop losses has been estimated at between €5 and 25 million per year in the Netherlands (Potting et al., 2013).

                    Control measures are often used against T. absoluta and chemical control is the most common tool used to suppress populations that suddenly grow in open-field tomato crops (Guedes and Picanço, 2012). Additional insecticide applications are necessary to fully control T. absoluta in the Netherlands, with an estimated increase in pest control-related costs of €4 million per year (Potting et al., 2013). In Turkey, the annual cost of chemical control of T. absoluta was approximately 160.7 million Euros (Oztemiz 2014). In South America, the introduction of T. absoluta in countries bordering the country of origin, the use of insecticides in tomato fields doubled per cultivation period. The increasing number of insecticide applications is mainly due to the problems linked to insecticide resistance in T. absoluta populations (Campos et al., 2014Roditakis et al., 2015). In most infested countries in Asia, information is not available on economic losses caused by T. absoluta infestation. The percentage of the damaged area has reached almost 100% in Iran and a loss of 35 million US dollars per year (Han et al., 2019).

                    Environmental Impact

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                    T. absoluta females have high reproductive potential and can produce more than 260 eggs during their lifetime (Uchoa-Fernandes et al., 1995). The pest can reach 12 generations in a year depending on biotic and abiotic factors in the infested region. Thus, productivity losses may reach 100% after the first infestation in the tomato crop. There may be a need to change the tomato crop to another crop bringing social changes and impact on habitat.

                    Huge insecticide selection pressure is obviously not compatible with most integrated pest management (IPM) programmes implemented in tomato systems. Consequently, there is potential disturbance of ecological services provided by pollinators and natural enemies exposed to pesticides (Biondi et al., 2012, 2013; Tomé et al., 2012a, 2015; Abbes et al., 2015).

                    Impact: Biodiversity

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                    There is a considerable loss of production in the tomato crop after the introduction of T. absoluta (Desneux et al., 2010). The main method of control is to reduce the population of the pest by the application of insecticides. However, in many infested regions, there are no insecticides recommended for control of T. absoluta. The use of insecticide is not recommended as it may affect the biodiversity, native species, and species of environmental conservation significance (Biondi et al., 2018).

                    Social Impact

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                    In some regions of Africa and Asia tomato is one of the few cash crops. The introduction of T. absoluta to the agroecosystem can have a great social impact (Sylla et al., 2017). In addition, the use of insecticides for the control of T. absoluta can affect the environment and human health in these areas (Guedes et al., 2019).

                    Risk and Impact Factors

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                    Invasiveness
                    • Invasive in its native range
                    • Proved invasive outside its native range
                    • Abundant in its native range
                    • Highly adaptable to different environments
                    • Capable of securing and ingesting a wide range of food
                    • Highly mobile locally
                    • Fast growing
                    • Has high reproductive potential
                    • Has high genetic variability
                    Impact outcomes
                    • Altered trophic level
                    • Changed gene pool/ selective loss of genotypes
                    • Ecosystem change/ habitat alteration
                    • Host damage
                    • Negatively impacts agriculture
                    • Negatively impacts cultural/traditional practices
                    • Negatively impacts livelihoods
                    • Reduced native biodiversity
                    • Threat to/ loss of native species
                    • Negatively impacts trade/international relations
                    Likelihood of entry/control
                    • Highly likely to be transported internationally accidentally
                    • Highly likely to be transported internationally illegally
                    • Difficult to identify/detect as a commodity contaminant
                    • Difficult to identify/detect in the field
                    • Difficult/costly to control

                    Uses List

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                    General

                    • Laboratory use

                    Detection and Inspection

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                    T. absoluta is easily found on tomato plants because it prefers the apical buds, flowers or new fruits, where the black frass is visible. When there is a severe attack it colonizes the leaves on the other parts of the plant. Mines are evident on attacked leaves (Imenes et al., 1990).

                    Females show a preference for oviposition on the apical and the median plant parts. First-instar larvae have a higher preference for apical and median parts of the plant, whereas the distribution of fourth-instar larvae was similar on all parts of plant (Galdino et al., 2015). Pupation is higher on the leaves and on apical plant parts, followed by the soil, main stem and fruits (Torres et al., 2001).

                    Similarities to Other Species/Conditions

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                    T. absoluta is morphologically similar to three other species in the family Gelechiidae: Keiferia lycopersicella (tomato pinworm), Tecia solanivora (potato tuber moth), and Phthorimaea operculella (potato tuber moth) (Biondi et al., 2018). 

                    Prevention and Control

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                    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.

                    Cultural Control

                    Agriculture management such as ploughing, manuring, irrigation, crop rotation, solarisation, as well as specific management by the elimination of symptomatic leaves and the destruction of infested tomato plants have all been used to control T. absoluta. Sequential planting with or near to other solanaceous crops that serve as shelter and food sources for T. absoluta such as potatoes, aubergine and pepper should be avoided (Sylla et al., 2019). The removal of alternative reservoir hosts such as nightshades (Solanum nigrum, Atropa belladonna, Solanum dulcamara) (Bawin et al., 2016) is strongly recommended before and during the cropping cycle. In greenhouses, one of the management tactics used to reduce the initial level of populations is to keep infested greenhouses closed after harvest to prevent the migration of adults to open-field crops. Alternating host crops, mainly tomato, potato and aubergine, with non-host cultures can ensure a long-term reduction in pest pressure (Sylla et al., 2019).

                    Chemical Control

                    The immediate threat to tomato production in Neotropical America led to intensive insecticide use against T. absoluta in the invaded areas, from 10-12 applications per cultivation cycle to more than 30 applications that required 4-6 weekly sprays (Guedes et al., 2019). However, the level of insecticide efficacy is often low due to the insect attacking multiple plant parts, and protection by the plant canopy, resulting in additional spraying and insecticide overuse (Desneux et al., 2011). The introduction of T. absoluta into the Afro-Eurasia regions was accompanied by extensive use of insecticides to keep the pest under control (Campos et al., 2017), resulting in a significant increase in both the average number of applications and pest control-related costs (Biondi et al., 2018). Initially, and due to the lack of specifically registered compounds for T. absoluta control, growers relied on broad-spectrum insecticides such as pyrethroids (Lietti et al., 2005; Balzan and Moonen, 2012; Siqueira et al., 2000; Mansour et al., 2018; Han et al., 2019). Since 2009, a wave of insecticide registrations for use against T. absoluta allowed a wider choice of products, depending on the country (Tomé et al., 2012b; Roditakis et al., 2013). These insecticide classes include organophosphates (chlorpyrifos), pyrethroids (deltamethrin, lambda-cyhalothrin, bifenthrin, permethrin), oxadiazines (indoxacarb), spinosyns (spinosad, spinetoram), avermectins (abamectin, emamectin benzoate), pyrroles (chlorfenapyr), benzoylureas (diflubenzuron, lufenuron, novaluron), diamides (chlorantraniliprole, flubendiamide), diacylhydrazines (chromafenozide, methoxyfenozide, tebufenozide), semicarbazones (metaflumizone), tetranortriterpenoids (azadirachtin) and nereistoxin analogs (cartap) (IRAC, 2014). Additionally, commercial formulations of some bio-insecticides based on Bacillus thuringiensis and Beauveria bassiana have been widely used on tomato crops, as they are often more compatible with natural enemies of T. absoluta (Biondi et al., 2012, 2013; Klieber and Reineke, 2016). Other bio-insecticides are also available, like limonene and borax, but exhibiting more limited use (Soares et al., 2019).

                    Semiochemicals

                    The use of pheromone-based strategies is recognized as an important monitoring and control technique for T. absoluta (Cocco et al., 2013; Megido et al., 2013). Significant advances have been made in the field of semiochemicals to cope with T. absoluta, especially sex pheromones which are important male attractants (Desneux et al., 2010). Although studies have reported the ability of T. absoluta to undergo parthenogenesis (Megido et al., 2012) or multiple mating (Garzia et al., 2012; Lee et al., 2014), effective mating disruption relies primarily on being able to prevent fecund females from immigrating into greenhouses. Pheromone traps are considered as the first line of defence against T. absoluta both in open fields and in greenhouses as they are used for monitoring and male annihilation purposes. Most of the IPM strategies developed or under development against T. absoluta utilise pheromones in combination with other control techniques such as light sources and water traps to mass trap both adult males and females simultaneously (Megido et al., 2013), mating disruption based on atmospheric saturation of the synthetic pheromone to reduce mating chances (Vacas et al., 2011; Cocco et al., 2013), the uses of homemade traps (translucent plastic cylinders, 9 × 11 cm, with a 4.5 × 6.5 cm opening) to reduce infestation (Lobos et al., 2013), or lure and kill techniques using a combination of a low amount of the synthetic sex pheromone of T. absoluta and an insecticide to reduce the male population (Witzgall et al., 2010; Cocco et al., 2013).

                    Inherited sterility (sterile males)

                    Inherited sterility programmes which involve releasing irradiated sterile males has been proposed as a possible method for control of T. absoluta (Cagnotti et al., 2012). This method used in over-flooding a ratio of 15:1 provided a significant reduction in the population of T. absoluta in a laboratory study (Cagnotti et al., 2016).

                    Biological Control

                    Several biocontrol agents are used to control T. absoluta in open-field and greenhouse tomato cultivation. Hemipteran predators, notably anthocorids, geocorids, mirids, nabids and pentatomids, have been identified as effective predators against T. absoluta in both native and invaded areas. The most common predators against T. absoluta are the mirid bugs Nesidiocoris tenuis, Macrolophus pygmaeus and Dicyphus spp. The predators Nesidiocoris tenuis and Macrolophus pygmaeus are commercially available and widely used in North Africa and Europe. However, they have different ecological characteristics and this should be assessed when they are applied in the T. absoluta-tomato system: N. tenuis populations can increase when relying only on the T. absoluta-tomato system (Mollá et al., 2014), whereas such a system is not fully suitable for M. pygmaeus (Jaworski et al., 2013; Sylla et al., 2016), which requires alternative prey to support population growth (Jaworski et al., 2015). Dicyphus spp. is an intermediate case, as it develops well using T. absoluta eggs as a sole prey but shows weak population growth on tomato when prey is lacking (Ingegno et al., 2013; Abbas et al., 2014).

                    Many parasitoids have been identified parasitizing T. absoluta in South America and in newly invaded regions. Mass rearing associated with inundative releases of several Trichogramma species proved technically viable as biocontrol agents in tomato greenhouses in Brazil, Spain and Egypt (Parra et al., 2004; Zappalà et al., 2012; 2013; El-Arnaouty et al., 2014). However, multiple releases are needed which compromise their economic usefulness against T. absoluta.

                    Bacillus thuringiensis (Bt)-based insecticide formulations have been used to control T. absoluta in its native and invaded regions (González-Cabrera et al., 2011). Several studies have demonstrated the efficacy of Bt in controlling T. absoluta. First-instar larvae are the most susceptible target and, on this basis, various commercially available formulations have been recommended for use without side effects on beneficial arthropods (Mollá et al., 2011). The biosurfactant Bacillus amyloliquefaciens AG1, caused serious histological damage in the larval midgut of T. absoluta (Ben Kheder et al., 2015) and the vegetative insecticidal protein B. thuringiensis Vip3Aa16, induced microvillus damage and epithelial cell rupture in the midgut of third-instar larvae of T. absoluta, cessation of feeding, body retraction, overall paralysis, and death of several larvae (Sellami et al., 2015). However, the efficiency of entomopathogenic fungi on T. absoluta has not been widely investigated. Several fungal species including Metarhizium anisopliae and Beauveria bassiana are reported to attack the eggs, larvae and adults of the pest. Studies have revealed up to 54% mortality of T. absoluta adults by M. anisopliae (Pires et al., 2009, 2010).

                    Entomopathogenic nematodes have been tested for the management of T. absoluta. Steinernema and Heterorhabditis spp., reduced infestation of T. absoluta on tomato plants by 87-95% under laboratory and greenhouse conditions (Batalla-Carrera et al., 2010). Steinernema carpocapsae and Heterorhabditis bacteriophora both provide high mortality the final instar of T. absoluta larvae in different soil types and temperatures. Moreover, both nematodes infected larvae within tomato leaf galleries providing control levels of 48-51% at high pest densities (Kamali et al., 2018). Laboratory and field trials revealed high larval mortality (78.6-100%) and low pupal mortality (10%) when Steinernema feltiae was evaluated against the pest (Garcia-del-Pino et al., 2013).

                    Host-Plant Resistance

                    The most promising genetic sources of resistance remain an intensively pursued management tactic, particularly since the 1990s (Guedes and Picanço, 2012). Among germplasm bank accessions of Solanum lycopersicum genetic sources are from wild tomato (Ecole et al., 2001; Maluf et al., 2010). Host-plant resistance was explored by developing tomato accessions with high zingiberene and/or acyl sugar contents resulting in low oviposition rates and larval feeding of T. absoluta (Azevedo et al., 2003; Maluf et al., 2010).

                    Gaps in Knowledge/Research Needs

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                    Studies on T. absoluta have increased over the past few years, specifically after the initial importation of the Chilean population into Spain. From this moment onwards, it was possible to focus efforts on elucidating the central origin, distribution, biology, ecology, and methods of controlling this pest.

                    Transgenic tomato plants expressing insecticidal proteins against specific lepidopterous pests could be developed. RNAi technology may also play an important role in specific gene silencing against T. absoluta. Thus, studies aiming to elucidate new tools to manage T. absoluta are proposed. 

                    References

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                    Abbas, S., Pérez-Hedo, M., Colazza, S., Urbaneja, A., 2014. The predatory mirid Dicyphus maroccanus as a new potential biological control agent in tomato crops. BioControl, 59(5), 565-574. doi: 10.1007/s10526-014-9587-6

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                    Links to Websites

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                    WebsiteURLComment
                    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.

                    Organizations

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                    France: European and Mediterranean Plant Protection Organization (EPPO), 21 boulevard Richard Lenoir F-75011, Paris, https://www.eppo.int/index

                    Italy: Food and Agriculture Organization (FAO), Viale delle Terme di Caracalla, 00153, Rome, http://www.fao.org/home/en/

                    Contributors

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                    30/11/20 Updated by:

                    Marianne Araújo Soares, Embrapa Agroenergy, Brasília, Brazil

                    Mateus Ribeiro Campos, INRAE, CNRS, UMR ISA, University Côte d’Azur, Nice, France

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