Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Meloidogyne enterolobii
(Pacara earpod tree root-knot nematode)

Castillo P and Castagnone-Sereno P, 2020. Meloidogyne enterolobii (Pacara earpod tree root-knot nematode). Invasive Species Compendium. Wallingford, UK: CABI. DOI:10.1079/ISC.33238.20210200738

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Meloidogyne enterolobii (Pacara earpod tree root-knot nematode)

Summary

  • Last modified
  • 10 December 2020
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Natural Enemy
  • Preferred Scientific Name
  • Meloidogyne enterolobii
  • Preferred Common Name
  • Pacara earpod tree root-knot nematode
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Nematoda
  •       Family: Meloidogynidae
  •         Genus: Meloidogyne
  • Summary of Invasiveness
  • The risk of introducing nonindigenous plant pathogens or pests into new areas is increasing rapidly due to globalization and the extensive trade and transport network now established within and among continents (...

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Pictures

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PictureTitleCaptionCopyright
Meloidogyne enterolobii (Pacara earpod tree root-knot nematode); rootknot symptoms on an ornamental Petunia spp. This nematode is considered a major economic pest of many horticultural and agronomic crops. It is particularly problematic because it can reproduce on and damage crop cultivars that are considered resistant to other root-knot nematode species. USA
TitleRoot-knot symptoms
CaptionMeloidogyne enterolobii (Pacara earpod tree root-knot nematode); rootknot symptoms on an ornamental Petunia spp. This nematode is considered a major economic pest of many horticultural and agronomic crops. It is particularly problematic because it can reproduce on and damage crop cultivars that are considered resistant to other root-knot nematode species. USA
Copyright©Jeffrey W. Lotz/Florida Department of Agriculture & Consumer Services/Bugwood.org - CC BY 3.0 US
Meloidogyne enterolobii (Pacara earpod tree root-knot nematode); rootknot symptoms on an ornamental Petunia spp. This nematode is considered a major economic pest of many horticultural and agronomic crops. It is particularly problematic because it can reproduce on and damage crop cultivars that are considered resistant to other root-knot nematode species. USA
Root-knot symptomsMeloidogyne enterolobii (Pacara earpod tree root-knot nematode); rootknot symptoms on an ornamental Petunia spp. This nematode is considered a major economic pest of many horticultural and agronomic crops. It is particularly problematic because it can reproduce on and damage crop cultivars that are considered resistant to other root-knot nematode species. USA©Jeffrey W. Lotz/Florida Department of Agriculture & Consumer Services/Bugwood.org - CC BY 3.0 US
Meloidogyne enterolobii (Pacara earpod tree root-knot nematode-RKN); damaged tomato roots.
TitleDamage symptoms
CaptionMeloidogyne enterolobii (Pacara earpod tree root-knot nematode-RKN); damaged tomato roots.
Copyright©Philippe Castagnone-Sereno-2014
Meloidogyne enterolobii (Pacara earpod tree root-knot nematode-RKN); damaged tomato roots.
Damage symptomsMeloidogyne enterolobii (Pacara earpod tree root-knot nematode-RKN); damaged tomato roots.©Philippe Castagnone-Sereno-2014
Meloidogyne enterolobii (Pacara earpod tree root-knot nematode); root-knots on guava (Psidium guajava). USA.
TitleRoot-knot symptoms
CaptionMeloidogyne enterolobii (Pacara earpod tree root-knot nematode); root-knots on guava (Psidium guajava). USA.
Copyright©Jeffrey W. Lotz/Florida Department of Agriculture & Consumer Services/Bugwood.org - CC BY 3.0 US
Meloidogyne enterolobii (Pacara earpod tree root-knot nematode); root-knots on guava (Psidium guajava). USA.
Root-knot symptomsMeloidogyne enterolobii (Pacara earpod tree root-knot nematode); root-knots on guava (Psidium guajava). USA.©Jeffrey W. Lotz/Florida Department of Agriculture & Consumer Services/Bugwood.org - CC BY 3.0 US

Identity

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Preferred Scientific Name

  • Meloidogyne enterolobii Yang & Eisenback, 1983

Preferred Common Name

  • Pacara earpod tree root-knot nematode

Other Scientific Names

  • Meloidogyne mayaguensis Rammah & Hirschmann, 1988

Summary of Invasiveness

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The risk of introducing nonindigenous plant pathogens or pests into new areas is increasing rapidly due to globalization and the extensive trade and transport network now established within and among continents (Hulme, 2009). Meloidogyne spp. are universally associated with vegetable production across the globe. Meloidogyne enterolobii is a highly pathogenic and aggressive invasive species emerging as an economically important species worldwide. As a root-knot nematode species, M. enterolobii can easily be transmitted with soil and plant material. Infested soil and growing media, plants for planting, bulbs and tubers from countries where M. enterolobii occurs are the most probable pathways of introduction into different regions. Soil attached to machinery, tools, footwear or plant products is also another possible pathway. The recent interception of this pest in several countries in Europe and the Mediterranean region (Germany, The Netherlands, UK) illustrates that it has the potential to enter different regions. In addition, M. enterolobii could survive under glasshouse conditions across regions with a sub-Mediterranean or a continental climate. Once root-knot nematodes have been introduced, it is generally difficult to control or eradicate them. Only in the EPPO region has this nematode been listed as a quarantine pest (EPPO A2 list No.361).

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Metazoa
  •         Phylum: Nematoda
  •             Family: Meloidogynidae
  •                 Genus: Meloidogyne
  •                     Species: Meloidogyne enterolobii

Notes on Taxonomy and Nomenclature

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Meloidogyne enterolobii was described from roots of pacara earpod tree (Enterolobium contortisiliquum) on Hainan Island in China (Yang and Eisenback, 1983). On the basis of female perineal patterns, it was preliminary identified as Meloidogyne incognita, and further analysis indicated some resemblance with the latter species; however, from a morphological point of view, the population was very different from M. incognita and any other described root-knot nematode species (Yang and Eisenback, 1983). A few years later, a new species of root-knot nematode was described from specimens recovered from galled roots of aubergines (Solanum melongena) in Puerto Rico, and named Meloidogyne mayaguensis (Rammah and Hirschmann, 1988). The authors indicated that 'M. mayaguensis superficially resembles M. enterolobii but differs distinctly from it in (some) morphological features' (Rammah and Hirschmann, 1988). In addition, the esterase phenotype of M. mayaguensis (VS1-S1) was identical to that of M. enterolobii (Esbenshade and Triantaphyllou, 1985; Rammah and Hirschmann, 1988). In 2012, Karssen et al. (2012) compared holo- and paratypes of both species and confirmed that M. mayaguensis should be considered as a junior synonym of M. enterolobii.

Description

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The original description was made from a population that seriously damaged pacara earpod trees (Enterolobium contortisiliqum) on Hainan Island in China (Yang and Eisenback, 1983), following a preliminary (false) identification from perineal patterns of females that indicated the presence of Meloidogyne incognita. The morphological characters from female, male and second-stage juvenile stages, as published in the original description, are detailed below.

Female

Body white, pear-shaped to globular, variable in size, with prominent neck variable in size, without posterior protuberance. Lip region not distinctly set off from neck. Labial disc and medial lips fuse to form labial cap. Hexaradiate labial framework distinct but weak; vestibule and vestibule extension prominent. Cephalids and hemizonids not observed. Position of excretory pore variable, often near metacorpus. Cuticular body annulations become progressively finer posteriorly. Stylet slender; conical portion slightly curved dorsally, tapering toward tip; cylindrical shaft, posterior end often enlarged. Knobs set off from shaft, distinct from each other, and divided longitudinally by groove so that each knob appears as two. Dorsal oesophageal gland orifice (DGO) 4-6 µm from base of stylet knobs; orifice branches into three channels; dorsal gland ampulla large. Subventral gland orifices branched, located immediately posterior to enlarged lumen lining of metacorpus; subventral gland ampulla small but distinct. Oesophageal gland comprised of one large uninucleate dorsal oesophageal gland lobe; two small, nucleated subventral oesophageal gland lobes usually posterior to dorsal gland lobe but variable in position, shape and size; all three lobes overlap intestine ventrally. Two small, rounded, singly nucleated oesophago-intestinal cells located between metacorpus and intestine. Perineal pattern usually oval, with coarse and smooth striae; dorsal arch moderately high to high, often rounded, nearly square in some specimens. Lateral lines not distinct. Perivulval region generally free of striae; striae may occur on lateral sides of vulva. Striae on ventral area of pattern generally finer and smoother. Tail tip visible; phasmidial ducts large.

Male

Body translucent white, vermiform, tapering at both ends. Tail end more rounded than anterior end, twisting through 90° in heat-killed specimens. In lateral view, labial cap high and rounded, lip region only slightly set off from body. Hexaradiate labial framework moderately developed; vestibule and extension distinct. In SEM, stoma slit-like, prestoma hexagonal, surrounded by pit-like openings of six inner labial sensilla. Labial disc and medial lips fuse, forming elongate labial cap and labial disc slightly elevated above medial lips. Four labial sensilla marked on medial lips by shallow cuticular depressions. Amphid openings slit-like; lateral lips absent; head region not annulated; body annuli distinct. Lateral field begins near level of stylet knobs as two incisures; two additional incisures start near level of metacorpus; lateral field areolated, encircles tail. Stylet robust; cone straight, pointed; opening located several micrometres from tip. Shaft cylindrical; knobs large, rounded, distinctly set off from shaft; in some specimens each knob is divided longitudinally by groove so that each knob appears as two but not as pronounced as in female. Distance of GDO to stylet base long, orifice branched into three channels, ampulla poorly defined. Procorpus distinct; metacorpus elongate, oval with enlarged cuticular lumen lining; oesophago-intestinal junction indistinct, at leveI of nerve ring. Gland lobe variable in length, with two nuclei. Excretory pore far from anterior end, terminal duct long. Hemizonid 2-4 annuli anterior to excretory pore. One or two testes, usually outstretched. Spicules arcuate, with rounded base, single tip. Gubernaculum short and simple. Tail short and rounded. Phasmids small, pore-like, at level of cloaca. 

Second–Stage Juvenile (J2)

Body translucent white, vermiform, rather long, tapering at both ends with very long, narrow tail. Anterior end truncate; head region only slightly set off from body. Vestibule and extension more developed than remainder of hexaradiate cephalic framework. In SEM, stoma slit-like, located in oval prestoma, surrounded by six pore-like openings of inner labial sensilla. Medial lips and labial disc dumbbell-shaped in face view. Labial disc rounded, raised slightly above medial lips. Lateral lips large and triangular, lower than labial disc and medial lips. Posterior edge of one or both lateral lip may fuse with tile head region in some specimens. Elongate amphidial apertures located between labial disc and lateral lips. Lip region not annulated; body annuli distinct but fine. Lateral field beginning near level of procorpus as two lines; near metacorpus third line begins and shortly splits making four lines, running entire length of body before gradually decreasing to two lines which end near hyaline tail terminus, irregularly areolated. In LM, stylet delicate; cone straight, narrow, sharply pointed; shaft becomes slightly wider posteriorly; knobs large, rounded, separate from each other, set off from shaft. Distance of DGO to stylet long; orifice branched into three channels; ampulla indistinct. Procorpus faintly outlined; metacorpus oval with enlarged lumen lining; isthmus not clearly defined oesophago-intestinal junction difficult to observe. Gland lobe variable in length, with three equal-sized nuclei; overlaps intestine ventrally. Excretory pore distinct; hemizonid 1-2 annuli anterior to excretory pore, 3-5 annuli long; cuticle slightly raised over hemizonid. Tail very thin; annulations increase in size, become more irregular posteriorly. Hyaline tail terminus clearly defined; tail tip broad, bluntly rounded. Rectum dilated. A few fat droplets may occur in hyaline tail terminus. Phasmids small, difficult to observe, located posterior to anus.

Distribution

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M. enterolobii is largely distributed in regions with typical tropical climatic conditions, including Asia, Africa, Europe, South and Central America and the Caribbean. It has also been reported from areas of North America exhibiting a warmer climate, e.g., Florida and North Carolina (Kaur et al., 2006; Ye et al., 2013). Because of its thermal requirements, M. enterolobii will probably not survive in colder regions. However, it might be able to establish in Mediterranean climates or in greenhouses (e.g., the nematode was detected on vegetables in greenhouses in Switzerland; Kiewnick et al., 2008). M. enterolobii has been intercepted on several occasions in a few European countries in plant materials imported from tropical areas. Recently, it has been reported in several localities of Portugal (Santos et al., 2019).

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: 17 Feb 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

BeninPresent
Burkina FasoPresent, Localized
Congo, Democratic Republic of thePresent
Côte d'IvoirePresent
GambiaAbsent, Unconfirmed presence record(s)
KenyaPresent
MalawiPresent, Localized
MozambiquePresent
NigerPresent
NigeriaPresent
SenegalPresent
South AfricaPresent
TogoPresent

Asia

ChinaPresent
-FujianPresent
-GuangdongPresent
-GuangxiPresent
-HainanPresent
-HunanPresent
-LiaoningPresent
-ShandongPresent
-YunnanPresent
IndiaPresent, Localized
-Madhya PradeshPresent
-RajasthanPresent
-Tamil NaduPresent
-Uttar PradeshPresent
-UttarakhandPresent
SingaporeAbsent, Eradicated
ThailandPresent, Localized
VietnamPresent

Europe

BelgiumAbsent, Intercepted only
FranceAbsent, Formerly present
NetherlandsAbsent, Intercepted onlyAbsent, intercepted only, confirmed by survey. 75 survey observations in 2012.
PortugalPresent, Few occurrences
SwitzerlandPresent, Few occurrences2008

North America

Costa RicaPresent
CubaPresent, Widespread
El SalvadorPresent
GuadeloupePresent
GuatemalaPresent
HondurasPresent
MartiniquePresent
MexicoPresent
NicaraguaPresent
Puerto RicoPresent, Widespread
Trinidad and TobagoPresent, Localized
United StatesPresent, Localized
-FloridaPresent
-North CarolinaPresent, Localized
-South CarolinaPresent, Few occurrences2018

South America

BrazilPresent, Widespread
-AlagoasPresent2010
-BahiaPresent
-CearaPresent
-Espirito SantoPresent
-GoiasPresent
-MaranhaoPresent2008
-Mato GrossoPresent
-Mato Grosso do SulPresent
-Minas GeraisPresent2007
-ParanaPresent
-PernambucoPresent
-PiauiPresent
-Rio de JaneiroPresent
-Rio Grande do NortePresent
-Rio Grande do SulPresent
-Santa CatarinaPresent
-Sao PauloPresent
-TocantinsPresent2009
VenezuelaPresent

History of Introduction and Spread

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M. enterolobii and the fact that it has been intercepted approximately 10 times from 1991 to 2007 in the Netherlands (although the identity of the nematode could only be confirmed in 2007). The Dutch NPPO intercepted M. enterolobii in 1991 in plants of Cactus sp. imported from South Africa; in 1993 and 1994 in plants of Syngonium sp. imported from Togo; in 1999 in plants of Ficus sp. imported from China; in 2004 in plants of Ligustrum sp. imported from China; in 2006 in plants of Brachychiton sp. imported from Israel; and in 2006 and 2008 in plants of Rosa sp. imported from South Africa and China (Netherlands Food and Consumer Product Safety Authority, 2008). The presence of M. enterolobii has been reported in glasshouses in France (Blok et al., 2002) and Switzerland (Kiewnick et al., 2008) which clearly demonstrates that there are pathways for the introduction of this pest into the EPPO region.

Risk of Introduction

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The risk of introducing nonindigenous plant pathogens or pests into new areas is increasing rapidly due to globalization and the extensive trade and transport network now established within and among continents (Hulme, 2009). As a root-knot nematode species, M. enterolobii can easily be transmitted with soil and plant material. Infested soil and growing media, plants for planting, bulbs and tubers from countries where M. enterolobii occurs are the most probable pathways of introduction into different regions. Soil attached to machinery, tools, footwear or plant products is also another possible pathway. The recent interception of this pest in several countries in Europe and the Mediterranean region (Germany, The Netherlands, UK) illustrates that it has the potential to enter different regions. In addition, M. enterolobii could survive under glasshouse conditions across regions with a sub-Mediterranean or a continental climate. Once root-knot nematodes have been introduced, it is generally difficult to control or eradicate them. Only in the EPPO region has this nematode been listed as a quarantine pest (EPPO A2 list No.361).

Hosts/Species Affected

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M. enterolobii is considered to be a highly polyphagous species, with a host range similar to that of Meloidogyne incognita (Yang and Eisenback, 1983). The most frequently recorded hosts include many vegetables, e.g., tomato, pepper and watermelon (Yang and Eisenback, 1983; Rammah and Hirschmann, 1988) but also guava (Gomes et al., 2011), ornamental plants (Brito et al., 2010) and weeds (Rich et al., 2009). Of particular concern is the ability of M. enterolobii to develop on crop genotypes carrying resistance to the major Meloidogyne species, among which are resistant cotton, sweet potato, tomatoes (Mi-1 gene), potato (Mh gene), soyabean (Mir1 gene), bell pepper (N gene), sweet pepper (Tabasco gene) and cowpea (Rkgene) (Yang and Eisenback, 1983; Fargette and Braaksma, 1990; Berthou et al., 2003; Brito et al., 2007; Cetintas et al., 2008). Very few crop species have been recorded as non-hosts for M. enterolobii, including grapefruit, sour orange, garlic and peanut (Rodriguez et al., 2003; Brito et al., 2004).

Host Plants and Other Plants Affected

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Plant nameFamilyContextReferences
AbelmoschusMalvaceaeUnknown
Angelonia angustifoliaPlantaginaceaeUnknown
  • Kaur et al. (2006)
Apium graveolens (celery)ApiaceaeUnknown
Artocarpus heterophyllus (jackfruit)MoraceaeOther
Bidens pilosa (blackjack)AsteraceaeUnknown
Byrsonima cydoniifoliaMalpighiaceaeOther
Callistemon (Bottle brush)MyrtaceaeOther
    Callistemon citrinus (lemon bottlebrush)MyrtaceaeUnknown
    Capsicum (peppers)SolanaceaeUnknown
    Capsicum annuum (bell pepper)SolanaceaeOther
    Capsicum chinense (habanero pepper)SolanaceaeUnknown
    Carica papaya (pawpaw)CaricaceaeOther
      Cereus hildmannianusCactaceaeOther
        Chrysanthemum (daisy)AsteraceaeUnknown
        Citrullus lanatus (watermelon)CucurbitaceaeOther
        Coffea (coffee)RubiaceaeMain
        Coffea arabica (arabica coffee)RubiaceaeUnknown
        Crotalaria juncea (sunn hemp)FabaceaeUnknown
        Cucumis sativus (cucumber)CucurbitaceaeMain
        Cucurbita pepo (marrow)CucurbitaceaeUnknown
        Daucus carota (carrot)ApiaceaeOther
        Dioscorea rotundataDioscoreaceaeOther
        Elaeocarpus decipiensElaeocarpaceaeOther
          Enterolobium contortisiliquum (tamboril)FabaceaeMain
          Erechtites hieraciifolius (American burnweed)AsteraceaeUnknown
          Euphorbia puniceaEuphorbiaceaeOther
          Glycine max (soyabean)FabaceaeMain
          Gossypium hirsutum (Bourbon cotton)MalvaceaeOther
          Ipomoea batatas (sweet potato)ConvolvulaceaeMain
          Lactuca sativa (lettuce)AsteraceaeUnknown
          MalpighiaMalpighiaceaeOther
            Malpighia emarginataMalpighiaceaeUnknown
            Manihot esculenta (cassava)EuphorbiaceaeOther
              Maranta arundinacea (arrowroot)MarantaceaeMain
              Momordica charantia (bitter gourd)CucurbitaceaeUnknown
              Morus (mulberrytree)MoraceaeHabitat/association
                Morus celtidifoliaUnknown
                Morus nigra (black mulberry)MoraceaeOther
                Musa (banana)MusaceaeUnknown
                Musa acuminata (wild banana)MusaceaeUnknown
                Musa spp.MusaceaeOther
                  Nicotiana tabacum (tobacco)SolanaceaeOther
                  Oeceoclades maculata (monk orchid)OrchidaceaeUnknown
                  Paulownia elongata (elongate paulownia)ScrophulariaceaeUnknown
                  Phaseolus vulgaris (common bean)FabaceaeMain
                  Physalis peruviana (Cape gooseberry)SolanaceaeOther
                    Piper nigrum (black pepper)PiperaceaeUnknown
                    Prunus persica (peach)RosaceaeUnknown
                    Psidium guajava (guava)MyrtaceaeMain
                    Solanum lycopersicum (tomato)SolanaceaeMain
                    Solanum lycopersicum var. cerasiformeUnknown
                    Solanum melongena (aubergine)SolanaceaeMain
                    Solanum pseudocapsicum (Jerusalem-cherry)SolanaceaeOther
                    Solanum quitoense (naranjilla)SolanaceaeOther
                      Solanum tuberosum (potato)SolanaceaeMain
                      Stenocereus queretaroensisUnknown
                      Vigna unguiculata (cowpea)FabaceaeUnknown
                      Zingiber officinale (ginger)ZingiberaceaeOther
                      • Xiao et al. (2018)
                      Ziziphus jujuba (common jujube)RhamnaceaeOther

                      Biology and Ecology

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                      Life-Cycle

                      M. enterolobii is a sedentary endoparasite. Its life-cycle is very similar to other root-knot nematodes, and can be summarized briefly as follows. The worms hatch in the soil as second-stage, infective juveniles (J2s) and migrate towards the root of their host plant, which they invade in the zone of elongation. There, they migrate intercellularly, first to the root apex and then to the vascular cylinder, where permanent feeding sites (i.e., giant cells) are established. Now sedentary, J2s further undergo three successive moults to develop into adults. The saccate (pyriform) females remain sedentary, producing large egg masses that are extruded in a gelatinous matrix out of the root, while males (if any) migrate out of the plant tissues (Abad et al., 2003). The life-cycle of M. enterolobii takes 4-5 weeks under favourable conditions and females produce around 400-600 eggs.

                      Reproduction

                      The reproduction of M. enterolobii is by mitotic parthenogenesis and the somatic chromosome number is 2n = 44-46. Most oocytes advance to metaphase and telophase soon after they have entered the uterus and show no extended prophase stage (Yang and Eisenback, 1983).

                      Climate

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                      ClimateStatusDescriptionRemark
                      Af - Tropical rainforest climate Preferred > 60mm precipitation per month
                      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) Preferred < 860mm precipitation annually
                      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)
                      Ds - Continental climate with dry summer Tolerated Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)

                      Pathway Causes

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                      CauseNotesLong DistanceLocalReferences
                      Crop productionrare Yes
                      Horticulturerare Yes

                      Pathway Vectors

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                      VectorNotesLong DistanceLocalReferences
                      AircraftRare, eggs, J2 and females Yes

                      Plant Trade

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

                      Wood Packaging

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                      Wood Packaging not known to carry the pest in trade/transport
                      Loose wood packing material
                      Processed or treated wood
                      Solid wood packing material with bark
                      Solid wood packing material without bark

                      Impact Summary

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

                      Economic Impact

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                      M. enterolobii is considered as a very damaging pest because of its wide host range, high reproduction rate and the induction of large galls (Castagnone-Sereno, 2012). Although few detailed studies are available, M. enterolobii is referred to as a highly aggressive species (i.e., a very successful parasitic species with high infestation rate on the roots of host plants) and induces more severe root galling than other root-knot nematode species. In a microplot experiment, tomato yield losses of up to 65% have been observed (Cetintas et al., 2007). In two greenhouses in Switzerland, yield losses of up to 50% and severe stunting of tomato rootstocks and cucumber were observed (Kiewnick et al., 2008). In heavily infested areas, cultivation may become unviable, as exemplified for guava in Brazil (Carneiro et al., 2007). In okra (Abelmoschus esculentus), Silva et al. (2019) verified the pathogenicity of this nematode under controlled conditions.

                      Risk and Impact Factors

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                      Invasiveness
                      • Invasive in its native range
                      • Proved invasive outside its native range
                      • Has a broad native range
                      • Abundant in its native range
                      • Highly adaptable to different environments
                      • Long lived
                      • Gregarious
                      • Has propagules that can remain viable for more than one year
                      • Reproduces asexually
                      Impact outcomes
                      • Host damage
                      • Negatively impacts agriculture
                      • Negatively impacts cultural/traditional practices
                      • Damages animal/plant products
                      Impact mechanisms
                      • Induces hypersensitivity
                      • Interaction with other invasive species
                      • Parasitism (incl. parasitoid)
                      • Pathogenic
                      • Rapid growth
                      • Rooting
                      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

                      Diagnosis

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                      Isoenzymes

                      A species-specific esterase phenotype (VS1-S1) with two major bands has been described for M. enterolobii, while occasionally, one of these bands could resolve into two minor bands (Esbenshade and Triantaphyllou, 1985; Carneiro et al., 2000). One very strong band and two other weak bands of Mdh (malate dehydrogenase) activity were observed in isolates. However, these two minor bands require a large amount of homogenates from several females for their detection (Brito et al., 2004).However, the limitation of this technique is that J2s cannot be reliably diagnosed, which hinders its use in e.g., routine examination of soil samples.

                      Molecular identification

                      In recent years, a number of molecular protocols have been developed that proved to be efficient in differentiating M. enterolobii from the most common root-knot nematode species, based on the presence/absence and/or size of the amplicons in PCR reactions. Conversely to isoenzyme electrophoresis, the interest of such PCR methods is that they can be applied to all developmental stages of nematodes. The molecular targets chosen in the various protocols available mainly include mitochondrial DNA (Blok et al., 2002; Brito et al., 2004; Xu et al., 2004), ribosomal DNA (Adam et al., 2007), satellite DNA (Randig et al., 2009) and an anonymous SCAR marker (Tigano et al., 2010). Recently, loop-mediated isothermal amplification (LAMP) (Niu et al., 2012; He et al., 2013), real-time PCR with specific primers (Kiewnick et al., 2015; Braun-Kiewnick et al., 2016), and Recombinase Polymerase Amplification assays were developed targeting the IGS rRNA gene of M. enterolobii (Ju et al., 2019; Subbotin, 2019). M. enterolobii contains divergent genome copies, but these arose from a different progenitor from the one of the M. incognita-group, representing an independent origin of apomixes (Szitenberg et al., 2017).

                      Detection and Inspection

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                      Similar to other root-knot nematode species, M. enterolobii induces typical galls on the roots of infected plants. In case of severe attacks, extremely large and numerous galls can be found (Cetintas et al., 2007). Above-ground symptoms include stunted growth, wilting, leaf yellowing and deformation of plant organs. Overall, crop yield is reduced both qualitatively and quantitatively. In addition, M. enterolobii infestation may favour attacks of roots by secondary plant pathogens.

                      The presence of M. enterolobii in infested soil and plant material can be determined after extraction of the nematodes using conventional methods and microscopic examination. However, as morphological characters often overlap in root-knot nematode species, misidentification of species using morphology as the only criteria may occur. Alternatively, the use of biochemical and molecular tools, such as esterase profiling and DNA-based markers, has proven to be a good complement to provide reliable diagnostics in most cases.

                      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.

                      As is the case for other root-knot nematodes, general management strategies against M. enterolobii rely on a combination of prevention and control practices to achieve effective reduction of the nematode population density below a damage threshold enabling sustainable crop production. Reviews describing such general practices are available in recent literature (e.g., Coyne et al., 2009; Nyczepir and Thomas, 2009).

                      Basically, taking into account the banning of most chemical nematicides, growing resistant crops or non-host plants currently represents the best method for reducing M. enterolobii populations. However, the list of non-host plants for this species is very limited. In addition, resistance genes active against the major tropical root-knot nematode species (i.e., M. incognita, M. javanica and M. arenaria) do not control M. enterolobii, for example, in the case the Mi-1, N and Rk genes from tomato, pepper and cowpea, respectively. Therefore, some efforts have been devoted in recent years to the identification of new sources of resistance to M. enterolobii, with some success in perennial crops. A decade ago, a screening experiment using high and durable inoculum pressure indicated that Ma genes in Myrobolan plum, known to control the main tropical root-knot nematode species, also control resistance to M. enterolobii (Rubio-Cabetas et al., 1999). In peach, commercial rootstocks carrying the RMia resistance gene were shown resistant to the nematode in greenhouse evaluation tests (Nyczepir et al., 2008; Daniel Esmenjaud, pers. comm.). In guava trees, whose cultivation may suffer high damage in cases of heavy infestations, resistance has recently been identified in Psidium spp. accessions (de Almeida et al., 2009; Freitas et al., 2014). Recently, the discovery of resistance of Psidium cattleianum to this nematode has increased its selective use as rootstock for guava (Macan and Cardoso, 2020). Oat, wheat and sorghum cultivars have been shown resistant to this nematode and can be recommended for crop rotation in areas infested with M. enterolobii (De Brida et al., 2018). Clearly, search for new sources of resistance to M. enterolobii, especially in vegetables and annual crops, and their introgression into cultivars of agronomic interest, currently represent a major challenge to plant breeders worldwide.

                      Another alternative to chemical nematicides is based on the use of biocontrol agents, and several organisms have been investigated for their antagonistic effects against M. enterolobii. However, although some show promise, the results of all these studies require validation in various field conditions before a biological agent active against M. enterolobii may be commercially released.

                      References

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                      02/04/20 Updated by:

                      Pablo Castillo, Institute for Sustainable Agriculture, Spanish National Research Council, CSIC, Avda. Menendez Pidal s/n, 14004-Cordoba, Spain.

                      30/10/14 Original text by:

                      Philippe Castagnone-Sereno, INRA, Institut Sophia Agrobiotech, UMR INRA1355/UNS/CNRS7254, 400 route des Chappes, BP167 – 06903 Sophia Antipolis Cedex, France.

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