EPPO Alert List: addition of Meloidogyne luci together with M. ethiopica
Considering the recent description of Meloidogyne luci as a new and distinct species, and the fact that all populations found in the EPPO region, initially identified as M. ethiopica (added to the EPPO Alert List in 2011) are now considered to be M. luci, the EPPO Secretariat estimated that both species could usefully be included in the EPPO Alert List, even if the difficulties in identifying them have created some confusion about their geographical distribution, host range and biology.
Meloidogyne ethiopica and Meloidogyne luci (root-knot nematodes)
Why
In 2003, a tropical root-knot nematode species, initially identified as ‘Meloidogyne ethiopica’ was found for the first time in a tomato greenhouse in Slovenia. As M. ethiopica is a polyphagous species which can multiply on many different types of plants (dicotyledons and monocotyledons), it was added in 2011 to the EPPO Alert List. In 2014, a morphologically similar species, M. luci, was described. In 2015 and 2017, molecular studies on populations of Meloidogyne species collected from a wide range of geographical origins and host plants showed that the populations found in the EPPO region and originally identified as M. ethiopica, corresponded in fact to M. luci. As both M. ethiopica and M. luci can damage a large number of economically important crops, the EPPO Secretariat decided that both M. ethiopica and M. luci should be included in the EPPO Alert List.
Where
M. ethiopica is a tropical root-knot species which was first described in 1968 in Southern Africa (Tanzania). Considering the recent confusion between M. ethiopica and M. luci, the geographical distribution is now rather uncertain.
EPPO region: absent (all populations of ‘M. ethiopica’ reported from Italy, Greece, Slovenia, and Turkey correspond to M. luci).
Africa: Ethiopia, Kenya, Mozambique, South Africa, Tanzania, Zimbabwe.
South America: Brazil (Distrito Federal, Minas Gerais, Parana, Rio Grande do Sul, Santa Catarina, Sao Paulo), Chile (detected in the Central Valley from Copiapo (north of Santiago) to Talca), Peru.
M. luci was first described in 2014 from different plant species in Brazil, Chile and Iran. In the EPPO region, M. luci (initially identified as ‘M. ethiopica’) was first found in 2003 on glasshouse tomatoes in 1 location (Dornberk) in Slovenia. All infested plants were destroyed and the nematode was no longer found. In 2009, M. luci (as ‘M. ethiopica’) was detected in 2 soil samples which had been collected from maize (Zea mays) and kiwifruit (Actinidia deliciosa) near Kavalla, Northern Greece. The situation of this nematode in Greece needs to be further investigated. In 2009, M. luci (as ‘M. ethiopica’) was also detected in Turkey in 2 tomato greenhouses of the University of Ondokuz Mayıs and in several commercial cucumber greenhouses in Çarşamba district (Samsun province). In 2013, M. luci was found in a single plot on potato (Solanum tuberosum) in Portugal. In the literature, there is a record of this nematode in Italy but data is lacking on its current situation.
EPPO region: Italy, Greece, Portugal (1 field), Slovenia (eradicated), Turkey.
South America: Brazil (Distrito Federal, Rio Grande do Sul, Parana), Chile, Guatemala.
Asia: Iran.
On which plants
M. ethiopica is a polyphagous pest that is able to parasitize at least 80 different host plants, including many economically important crops. Considering the recent confusion between M. ethiopica and M. luci, the following host plant list is now rather uncertain. In Africa and South America, M. ethiopica has been observed on many different cultivated species such as: Actinidia deliciosa (kiwi), Agave sisalana (sisal), Asparagus officinalis, Beta vulgaris (beetroot), Brassica oleracea (cabbages), Capsicum frutescens (chilli pepper), Citrullus lanatus (watermelon), Cucurbita spp., Ensete ventricosum (ensete), Glycine max (soybean), Lactuca sativa (lettuce), Nicotiana tabacum (tobacco), Phaseolus vulgaris (common bean), Polymnia sonchifolia (yacon), Solanum lycopersicum (tomato), Solanum tuberosum (potato), Vicia faba (faba bean), Vigna unguiculata (cowpea), Vitis vinifera (grapevine), as well as on trees (Acacia mearnsii) and weeds (Ageratum conyzoides, Datura stramonium, Solanum nigrum).
M. luci has been found on the following plant species: Abelmoschus esculentus (okra), Actinidia deliciosa (kiwifruit), Antirrhinum majus (snapdragon), Brassica oleracea var. italica (broccoli), Cucumis sativus (cucumber), Daucus carota (carrot), Glycine max (soybean), Hylotelephium spectabile (sedum), Lactuca sativa (lettuce), Lavandula angustifolia (lavender), Phaseolus vulgaris (common bean), Polymnia sonchifolia (yakon), Rosa sp. (rose), Solanum lycopersicum (tomato), Solanum tuberosum (potato), Vitis vinifera (grapevine). At least on bean, tomato, and soybean crops, symptoms of decline and stunting, as well as root galling have been reported.
Host range experiments have also showed that M. luci (as ‘M. ethiopica’) can also multiply on a large number of cultivated plants of economic importance, for example: Allium cepa (onion), Apium graveolens (celery), Fagopyrum esculentum (buckwheat), Helianthus annuus (sunflower), Hordeum vulgare (barley), Medicago sativa (lucerne), Oryza sativa (rice), Pisum sativum (pea), Prunus persica (peach), Solanum melongena (aubergine), Spinacia oleracea (spinach), Zea mays (maize).
Damage
As is the case with other root-knot nematodes, both M. ethiopica and M. luci damage plants by affecting the development of their root systems which are distorted by multiple small and large galls and devoid of fine roots. Affected plants can also show above ground symptoms such as stunting and wilting. In Brazil and Chile, M. ethiopica is considered to be a damaging species on kiwi and grapevine, as infestations lead to a reduction of plant growth, fruit size and quality. In Brazil, it has also been reported to cause multiple galls on potato root systems, as well as protuberances on tubers. Data is generally lacking on the extent of damage and the economic impact these nematodes may cause on their different host plants. Data is also lacking on their biology.
Transmission
As a root-knot nematode species, both M. ethiopica and M. luci can easily be transmitted with soil and plant root material. In Chile, it is suspected that movements of contaminated grapevine nursery stock have probably resulted in serious infestations in various vineyards. In Brazil, it is also suggested that M. ethiopica was introduced in 1989 to Rio Grande do Sul on kiwi seedlings imported from Curicó (Chile), and that the pest was then moved to Distrito Federal on infested bulbs of Polymnia sonchifolia (yacón or Peruvian ground apple) from Rio Grande do Sul.
Pathway
Infested soil and growing media, plants for planting, bulbs and tubers from countries where M. ethiopica or M. luci occur are the most probable pathways to introduce and spread these pests into the EPPO region. Soil attached to machinery, tools, footwear, or plant products is also another possible pathway.
Possible risks
Both M. ethiopica and M. luci are polyphagous species and many of their host plants are of economic importance to the EPPO region as they are cultivated as arable, vegetable, ornamental or fruit crops. The detection of M. luci in the EPPO region clearly demonstrated that it has the potential to enter the region, although its pathway of introduction remains unknown. Studies had shown that, despite its probable tropical origin, M. luci (as ‘M. ethiopica’) has the potential to survive outdoors under a continental climate (hot summers and cold winters) even in areas where soil temperatures fall below zero during winter, as well as under a sub-Mediterranean climate (hot summers and mild winters). More studies on the potential of establishment of M. ethiopica in the EPPO region would be needed but its similarities with M. luci suggest that it may also survive under temperate conditions. Once root-knot nematodes have been introduced, it is in general difficult to control or eradicate them. The confusion between M. ethiopica and M. luci underlines the difficulties faced in establishing a reliable identification between morphologically similar species. Considering the wide host range of both species and their probable (or verified) ability to establish under temperate conditions, it seems desirable to avoid the introduction of M. ethiopica and the spread of M. luci in the EPPO region.
EPPO RS 2011/004, 2013/006, 2014/007, 2016/212, 2017/216, 2017/217, 2017/218
Panel review date 2017-03 Entry date 2011-01
Sources
Aballay E, Persson P, Mårtensson A (2009) Plant-parasitic nematodes in Chilean vineyards. Nematropica 39, 85-97.
Aydınlı G, Mennan S, Devran Z, Širca S, Urek G (2013) First report of the root-knot nematode Meloidogyne ethiopica on tomato and cucumber in Turkey. Plant Disease 97(9), p 1262.
Bellé C, Brum D, Groth MZ, Barros DR, Kaspary TE, Schafer JT, Gomes CB (2016) First report of Meloidogyne luci parasitizing Glycine max in Brazil. Plant Disease 100(11), p 2174.
Carneiro RMDG, Almeida MRA (2005) [Record of Meloidogyne ethiopica Whitehead on yacon and tomato plants in Brasília, DF, Brazil]. Nematologia 29(2), 285-287 (in Portuguese) (abst.).
Carneiro RMDG, Almeida MRA, Cofcewicz ET, Magunacelaya JC, Aballay E (2007) Meloidogyne ethiopica, a major root-knot nematode parasitising Vitis vinifera and other crops in Chile. Nematology 9, 635-641.
Carneiro RMDG, Correa VR, Almeida MRA, Gomes ACMM, Deimi AM, Castagnone-Sereno P, Karssen, G (2014) Meloidogyne luci n. sp. (Nematoda: Meloidogynidae), a root-knot nematode parasitising different crops in Brazil, Chile and Iran. Nematology 16(3), 289-301.
Carneiro RMDG, Gomes CB, Almeida MRA, Gomes ACMM, Martins I (2003) [First record of Meloidogyne ethiopica Whitehead, 1968 on kiwi in Brazil and reaction on different plant species]. Nematologia Brasileira 27, 151-158.
Carneiro RMDG, Randing O, Almeida MRA, Gomes ACMM (2004) Additional information on Meloidogyne ethiopica Whitehead, 1968 (Tylenchida: Meloidogynidae), a root-knot nematode parasitising kiwi fruit and grape-vine from Brazil and Chile. Nematology 6, 109-123.
Castro JMC, Lima RD, Carneiro RMDG (2003) [Isoenzymatic variability in Brazilian populations of Meloidogyne spp. from soybean]. Nematologia Brasileira 27(1), 1-12 (in Portuguese).
Conceição IL, Tzortzakakis EA, Gomes P, Abrantes I, da Cunha MJ (2012) Detection of the root-knot nematode Meloidogyne ethiopica in Greece. European Journal of Plant Pathology 134(3), 451-457.
Golden AM (1992) Large phasmids in the female of Meloidogyne ethiopica Whitehead. Fundamental and Applied Nematology 15(2), 189-191.
Gomes CB, Carbonari JJ, Medina IL, Lima DL (2005) [Survey of Meloidogyne ethiopica in kiwi in Rio Grande do Sul State, Brazil, and its association with Nicotiana tabacum and Sida rhombifolia]. Abstract of a paper presented at the XXV Congresso Brasileiro de Nematologia (Piracicaba, BR, 2005-02-13/18). Nematologia Brasileira 29(1), p 114.
Hunt DJ, Handoo ZA (2009) Taxonomy, Identification and Principal Species. In: RN Perry, M Moens, JL Starr (Eds.) Root-knot nematodes, pp. 55-88. CABI, Wallingford (GB).
Janssen T, Karssen G, Verhaeven M, Coyne D, Bert W (2015) Mitochondrial coding genome analysis of tropical root-knot nematodes (Meloidogyne) supports haplotype based diagnostics and reveals evidence of recent reticulate evolution. Scientific Reports 6, 22591. DOI: 10.1038/srep22591
Lima EA, Mattos JK, Moita AW, Carneiro RG, Carneiro RMDG (2009) Host status of different crops for Meloidogyne ethiopica control. Tropical Plant Pathology 34, 152-157.
Machado ACZ, Dorigo OF, Carneiro RMDG, de Araujo Filho JV (2016) Meloidogyne luci, a new infecting nematode species on common bean fields at Paraná State, Brazil. Helminthologia 53(2), 207-210.
Mandefro W, Dagne K (2000) Cytogenetic and esterase isozyme variation of root-knot nematode populations from Ethiopia. African Journal of Plant Protection 10, 39-47.
Murga-Gutierrez SN, Colagiero M, Rosso LC, Finetti Sialer MM, Ciancio A (2012) Root-knot nematodes from asparagus and associated biological antagonists in Peru. Nematropica 42(1), 57-62.
O’Bannon JH (1975) Nematode survey in Ethiopia. Institute of Agricultural Research, Addis Ababa, Ethiopia. FAO Rome, 29 pp.
Personal communication with Dr S. Širca (Agricultural Institute of Slovenia, 2011-01).
Širca S, Urek G, Karssen G (2004) First report of the root-knot nematode Meloidogyne ethiopica on tomato in Slovenia. Plant Disease 88(6), p 680.
Somavilla L, Gomes CB, Antunes LEC, de Oliveira RP, Carneiro RMDG (2009) [Reaction of different fruit crops to Meloidogyne ethiopica]. Nematologia Brasileira Piracicaba 33(3), 252-255 (in Portuguese).
Strajnar P, Širca S, Geric Stare B, Urek G (2009) Characterization of the root-knot nematode, Meloidogyne ethiopica Whitehead, 1968, from Slovenia. Russian Journal of Nematology 17, 135-142.
Strajnar P, Širca S, Knapič M, Urek G (2011) Effect of Slovenian climatic conditions on the development and survival of the root-knot nematode Meloidogyne ethiopica. European Journal of Plant Pathology 129(1), 81-88.
Tigano MS, Carneiro RMDG, Jeyaprakash A, Dickson DW, Adams BJ (2005) Phylogeny of Meloidogyne spp. based on 18S rDNA and the intergenic region of mitochondrial DNA sequences. Nematology 7(6), 851-862.
Whitehead AG (1968) Taxonomy of Meloidogyne (Nematoda: Heteroderidae) with description of four new species. Transactions of the Zoological Society of London 31, 263-401.
Whitehead AG (1969) The distribution of root-knot nematodes (Meloidogyne spp.) in tropical Africa. Nematologica 15, 315-333.