Skip to main content
. 2023 Jul 6;21(7):e08073. doi: 10.2903/j.efsa.2023.8073
Taxonomic information

Current valid scientific name: Meloidogyne mali

Synonyms: Meloidogyne ulmi

Name used in the EU legislation: –

Order: Rhabditia

Family: Meloidogynidae

Common name: apple root‐knot nematode

Name used in the Dossier: Meloidogyne mali

Group Nematodes
EPPO code MELGMA
Regulated status

Meloidogyne mali is included in the EPPO A2 list (EPPO, online_a) and was recently recommended for regulation as quarantine pest (EPPO, online_b).

Meloidogyne mali is quarantine pest in the US and Morocco (EPPO, online_a) and listed as a ‘pest of quarantine interest' in the Dominican Republic (EPPO, 2017); it is also regulated in Colombia, the Republic of Korea, Malaysia and Uruguay (EPPO, 2017). All Meloidogyne species are quarantine pests for Türkiye (EPPO, 2017).

Pest status in the UK

Meloidogyne mali is present in the UK in Southern England – two sites in Farnham and Surrey (Dossier Section 3.0) where it was found on elm trees in 2018, as consequence of introduction in the past of infected elms from the Netherlands (Prior et al., 2019).

According to the Dossier Section 5.0, the nematode is present in the UK: not widely distributed and not under official control.

Pest status in the EU

Meloidogyne mali is currently present in the EU in Austria (de Jong et al., online); it is also present in Belgium (Suwanngam and Wesemael, 2019), Italy (Palmisano and Ambrogioni, 2000) and the Netherlands (Ahmed et al., 2013), in all cases with few occurrences or restricted distribution (EPPO, online_c).

M. mali was detected in France (Ile de France) in 2016, but it was eradicated in 2021 (EPPO, online_c).

According to Ahmed et al. (2013) and EPPO (2017), M. mali may have a wider distribution in Europe, since elm plants growing in plots infested by the nematode in the Netherlands have been sent to other countries (Belgium, Denmark, France, Germany, Ireland, Italy, Spain, Slovakia, Romania, the UK) to carry out resistance tests against the Dutch Elm Disease (DED). These programmes started from the 80s of the last century (Prior et al., 2019).

Host status on Acer

Acer palmatum, A. pseudoplatanus, A. x freemanii, and Acer saccharinum, are host plants for Meloidogyne mali (EPPO, 2017; Kang et al., 2021).

There is no information on whether Acer platanoides may be hosts for M. mali.

PRA information Available pest risk assessments:
  • Risks to plant health posed by EU import of soil or growing media (EFSA PLH Panel, 2015);

  • A quickscan pest risk analysis for the Meloidogyne mali (Pylypenko, 2016);

  • Pest Risk Analysis for Meloidogyne mali, apple root‐knot nematode (EPPO, 2017);

  • Scientific opinion on the commodity risk assessment of Malus domestica plants from United Kingdom (EFSA PLH Panel, 2023);

  • UK Risk Register Details for Meloidogyne mali (DEFRA, online).

Other relevant information for the assessment
Biology

Meloidogyne mali is a root‐knot nematode inducing root galls on host plants; it is native to Asia (Japan), introduced decades ago to Europe and more recently also to the US (EPPO, 2017; Eisenback et al., 2017) and to the Republic of Korea (Kang et al., 2021).

When found in Europe in 2000, the nematode was initially described as a new species, Meloidogyne ulmi (Palmisano and Ambrogioni, 2000) and elms remained long time the only known host plants. The synonymy with the well‐known species M. mali was found later, after comparison in the Netherlands with living material from Japan (Ahmed et al., 2013).

Meloidogyne mali develops through three stages: eggs, juveniles (four stages) and adults, all living in the root galls. Adult males, second‐stage juveniles and eggs can live also free in the soil (EPPO, 2017). Information on M. mali biology mainly come from Malus sp. in Japan where the nematode and has one generation per year and the life cycle lasts 18–22 weeks. However, it is known that Meloidogyne species can frequently have more generations per year depending on the temperature and the feeding on perennial plants. Only few specific information on the life cycle of M. mali is available. Unlike similar species as M. chitwoodi and M. fallax which are parthenogenetic, Meloidogyne mali reproduces sexually. Like all Meloidogyne root‐knot nematodes, it deposits eggs in gelatinous sacs on the surface of galls or within them (EPPO, 2017; EFSA, 2019); in Japan, the minimum hatching temperature range of M. mali eggs is 10–15°C (optimal 20–33°C) (EPPO, 2017). As usual in Meloidogyne species, the infective second‐stage juveniles move in the soil and attack the roots penetrating behind the root cap. They start to feed on cortical tissues inducing the formation of giant cells that cause swelling and finally root galls. After moulting, adults develop from the last juvenile stage; females remain into the roots where they lay eggs in a gelatinous matrix, while males leave the galls (EFSA, 2019). It is not clear in what extent the nematode can survive frost conditions during winter. Meloidogyne mali can probably overwinter in the roots of plants growing outdoors, possibly as young females, given that egg‐laying females have been observed in early March (EPPO, 2017). In the US, the nematode seems able to survive at minimum winter temperature of −6°C (Pylypenko, 2016). Although Meloidogyne species are known not forming cysts to resist to the absence of host plants for long time, M. mali can survive for at least 2 years in root fragments in the soil after removal of infected trees; it is not known, however, if the nematode can also have a diapause period (EPPO, 2017).

All Meloidogyne are strictly associated with the roots of plants and are known to be sedentary species, moving in the soil 1–2 m maximum per year, and spread through the roots depending on their size, type of soil, water availability and other parameters (EFSA, 2019). As other species of root‐knot nematodes, the spread on medium–long distance of Meloidogyne mali is by passive transport, and possible pathways are mainly plants for planting with infected roots, soil and growing media and also contaminated tools and machinery (EPPO, 2017).

Symptoms Main type of symptoms

Plants infected by Meloidogyne mali show root‐knot galls on roots. The galls can be of different size also depending on the hosts and are always visible to the naked eye (0.5–2 cm in diameter) (EPPO, 2018). When a severe root infection occurs, as consequence of the developing of large number of galls the root system can be damaged, reducing uptake of water and minerals and causing symptoms on above‐ground part of plants. Common symptoms are little growth of primary shoots and increase of secondary shoots, leaf fall and general reduction of growth.

No specific information about symptoms on Acer sp. was found.

Presence of asymptomatic plants Plants infected by Meloidogyne mali can remain asymptomatic. Damage on above‐ground part of plants goes often unnoticed in early infection stage or when underground attack on roots is light. 30‐year‐old elms gravely infected in the root system were uprooted by wind without any symptom on the crown or foliage (EPPO, 2017).
Confusion with other pests

Plants infected by Meloidogyne mali appear similar to plants infected by other nematode species or root pathogens living in the soil.

The identification of the nematode is not possible on the basis of sole galls. M. mali juveniles and adults are morphologically similar to other Meloidogyne nematodes. For identification to species level, laboratory tests on morphometric characters, electrophoresis or sequencing/DNA barcoding are needed (EPPO, 2018).

Host plant range

Meloidogyne mali is a polyphagous nematode feeding on roots of several species of trees, shrubs and herbaceous plants.

Some important woody hosts of M. mali are Acer x freemani, A. palmatum. A. pseudoplatanus, Castanea crenata, Euonymus kiautschovicus, E. fortunei, Fagus sylvatica, Lagerstroemia indica, Malus pumila, Morus alba, Prunus serrulata, Quercus robur, Sorbus aucuparia, Taxus baccata, Ulmus glabra, U. parvifolia, Vitis vinifera, Zelkova serrata (EPPO, 2017; DEFRA, online; Ferris, online).

Common herbaceous hosts are Dryopteris filix‐mas, D. carthusiana, Geranium robertianum, Geum coccineum, Impatiens parviflora, Rosa sp., Rubus fruticosus, Taraxacum officinale, Trifolium repens and Urtica dioica (EPPO, 2017; DEFRA, online).

For a complete list of hosts, see EPPO (2017) and DEFRA (online).

Reported evidence of impact

Only poor information on economic impact caused by Meloidogyne mali is available. In Japan, damage on Malus and Morus (15–43% growth reduction) was reported only following inoculation experiments.

In Italy, slowly declining elms were observed (Palmisano and Ambrogioni, 2000). In the UK, M. mali was only found in elms killed by DED (Prior et al., 2019). Roots damaged by M. mali may be also attacked by secondary pathogen agents. On elm trees in the Netherlands, the infection by M. mali caused detriment of stability with uprooting by wind in urban areas (EPPO, 2017).

No specific data about damage on Acer was found.

Evidence that the commodity is a pathway Meloidogyne mali can travel with plants for planting; therefore, they are possible pathways of entry for the nematode. The pest has been intercepted in China in 2013 and 2020 on Acer palmatum and in 2015 on Lagerstroemia indica, in both cases on plants imported from Japan (EPPO, 2017; GenBank, online). In the period 1995–December 2022, there have been several interceptions of Meloidogyne species in the EU from Japan, mostly on bonsais, including on hosts of M. mali as Acer palmatum, although in these hosts, the nematode was never identified at species level.
Surveillance information

According to the Dossier Section 5.0, Meloidogyne mali is not under official surveillance, as does not meet criteria of quarantine pest for Great Britain.

A survey was conducted to determine the extent of Meloidogyne mali presence in Surrey; all of the samples outside the two sites where the nematode was found in 2018 were negative, indicating that it has not spread off the sites (Dossier Section 3.0).

A containment approach is being implemented in the two sites. No movement of soil from the sites is allowed. No movement of host plants from the sites is allowed. Staff and contractors coming into contact with host plants or soil on sites must remove soil from footwear and equipment before leaving the sites. Only non‐hosts should be planted at the sites (Dossier Section 3.0).