Preferred name: Nacobbus aberrans sensu lato
Authority: (Thorne) Thorne & Allen
Taxonomic position: Animalia: Nematoda: Chromadorea: Rhabditida: Pratylenchidae
Other scientific names: Anguillulina aberrans Thorne, Nacobbus batatiformis Thorne & Schuster, Nacobbus serendipiticus bolivianus Lordello, Zamith & Boock, Nacobbus serendipiticus Franklin
Common names in English: false root-knot nematode
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Notes on taxonomy and nomenclature EPPO Categorization: A1 list
EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: NACOBA

Nacobbus aberrans s.l. is highly polyphagous, attacking at least 84 plant species of 24 families, including crops, native plants, and weeds (Manzanilla-López et al., 2002; Doucet & Lax, 2005; EPPO, 2009). Potato, tomato, pepper, sugarbeet and bean are the most economically significant hosts. Weeds can function as a permanent source of inoculum in cultivated crops or as reservoirs in the absence of the culture (Inserra et al., 1984; Doucet & Lax, 2005). Nematode populations from different geographic origins may show distinct behaviours when interacting with the same plant species or cultivar. This indicates that certain populations possess the ability to invade and proliferate within roots of a given plant, while others are unable to infest them. Consequently, based on these host preferences, populations can be differentiated into groups, races, biotypes or pathotypes (Castiblanco et al., 1999; Manzanilla-López et al., 2002; Inserra et al., 2005; Franco & Main, 2008; Lax et al., 2011), which are associated with specific host ranges and geographic areas (EFSA PLH et al., 2018).

Host list: Amaranthus hybridus, Amaranthus hypochondriacus, Amaranthus quitensis, Amaranthus retroflexus, Amaranthus sp., Amaranthus spinosus, Anoda cristata, Atriplex confertifolia, Baccharis salicifolia, Bassia scoparia, Beta vulgaris, Brassica juncea, Brassica napus, Brassica nigra, Brassica oleracea, Brassica rapa subsp. sylvestris, Brassica rapa, Capsella bursa-pastoris, Capsicum annuum, Capsicum baccatum var. pendulum, Capsicum frutescens, Capsicum pubescens, Cestrum roseum, Chenopodiastrum murale, Chenopodium album, Chenopodium berlandieri var. berlandieri, Chenopodium quinoa, Cucumis sativus, Cucurbita maxima, Cucurbita pepo, Datura ferox, Datura stramonium, Daucus carota, Dysphania ambrosioides, Escobaria vivipara, Ipomoea batatas, Lactuca sativa, Malva parviflora, Nicotiana tabacum, Opuntia fragilis, Origanum vulgare, Oxalis tuberosa, Phaseolus vulgaris, Physalis sp., Pisum sativum, Plantago lanceolata, Portulaca oleracea, Raphanus sativus, Salsola kali, Senecio vulgaris, Sisymbrium irio, Solanum lycopersicum, Solanum melongena, Solanum tuberosum, Spergula arvensis, Spinacia oleracea, Stellaria media, Taraxacum officinale, Tribulus terrestris, Trifolium sp., Tropaeolum tuberosum, Ullucus tuberosus

The pest is indigenous to the American continent (Sher, 1970). Although quarantine records and interceptions of contaminated plant material have been reported in other countries, such as England, the Netherlands and Russia, there is so far no evidence of establishment of this nematode outside the Americas (Manzanilla-López et al., 2002).

North America: Mexico, United States of America (Arkansas, Colorado, Kansas, Montana, Nebraska, South Dakota, Utah, Wyoming)
South America: Argentina, Bolivia, Chile, Ecuador, Peru

The life cycle of Nacobbus aberrans s.l. has four juvenile stages (J1 inside the egg, J2-J4) and the adults (male, immature and mature female). The J2-J4 and immature female (filiform) are infective, migratory and endoparasitic stages and can be found inside the roots and/or in the soil. The immature female establishes near the central root cylinder, becoming a sedentary endoparasite with a fusiform body. Feeding and development is accompanied by histological changes and gall formation by the roots, and eggs are laid in a gelatinous matrix which protrudes from the root surface into the soil. Development can be completed in about 37-48 days at 22-24 °C and even extend up to almost a year (observed when the nematode infests potato tubers). J3 and J4 are able to survive for more than 10 months in a quiescent state under the lenticels of stored potato tubers (Costilla, 1985a). The nematode is adapted to a wide range of climatic conditions; it is resistant to low temperatures (below -10 °C) and above 30 °C (Manzanilla-López et al., 2002). Under laboratory conditions, N. aberrans s.l. survived after 4 months in infested roots and soil at -13 °C, and 8 months in air-dried soil (7-9% RH) (Jatala & Kaltenbach, 1979).

Symptoms

The galls are similar to those caused by the root-knot nematodes (Meloidogyne spp.) and it is not possible to differentiate these nematodes from N. aberrans s.l. based on this root symptom. Infested potato tubers do not show visible symptoms.

Morphology 

The genus Nacobbus is characterized by the females having a single ovary (two in Meloidogyne) and males having a bursa. Mature females in the root galls are fusiform with tapered posterior position contrasting with the rounded posterior end of Meloidogyne mature females. Although the Nacobbus mature female can be easily identified, the free mobile stages can be confused with other species, especially those of the family Pratylenchidae (Anthoine & Mugniéry, 2005). The immature female is vermiform and is found in roots and in soil. The tail of immature females and juveniles (J2-J4) is rounded whereas Meloidogyne J2 has a tapered tail. See also Manzanilla-López et al. (2002) and Lax et al. (2021).

Detection and inspection methods

The detection technique will depend on the type of material to be tested (roots, potato tubers, or soil samples). In roots, direct dissection of the galls can reveal the presence of fusiform females. Roots or potato peelings can be processed using the maceration-centrifugal-flotation (Coolen, 1979) or maceration-flotation method (Costilla, 1985b). During periods of temperature decline and drought, dormant stages of N. aberrans s.l. in soil can tolerate desiccation for 24 months. As a consequence, the nematode extraction from the soil using routine methods may be nil or very low. This makes it difficult to accurately assess the level of population density prior to sowing or transplanting a susceptible crop (Cristóbal et al., 2001). The main techniques for nematode detection in soil samples are Baermann funnel or its modification, flotation-centrifugation with sugar (Manzanilla-López et al., 2002) and ‘the closed bag method’ described by Ortuño et al. (1996). A molecular diagnostic method for detecting N. aberrans s.l. in soil and in potato tubers was developed by Atkins et al. (2005). More details are given in the EPPO diagnostic protocol EPPO (2009).

N. aberrans s.l. can be spread in contaminated potato tubers (Lax et al., 2013), as well as with the movement of infested plants and soil (EFSA PLH et al., 2018).

Economic impact

N. aberrans s.l. is ranked as one of the top ten nematode pests in the world (Jones et al., 2013). The impact on yield depends on different factors, such as population pathotype/group, initial density, climatic conditions, soil type, and the crop/cultivar selected (Lax et al., 2022). In the Andean region, it is one of the main pests of the potato crop, reducing yields by about 10-73% (Canto-Saenz et al., 1996; Franco et al., 1996). Tomato production is reduced by around 60-75% in Ecuador (Corrales Arango, 2007) and by 12-83% in Mexico (Cristóbal-Alejo et al., 2006). In sugarbeet, losses range between 10-20% in the USA (Inserra et al., 2005), and up to 36% on bean in Mexico (Manzanilla-López et al., 2002).

Control

Nematicides alone do not effectively reduce populations of N. aberrans s.l. (Manzanilla-López et al., 2002). The main strategies that need to be rationally applied include: crop rotation, use of tolerant/resistant cultivars, use of trap and antagonistic plants, avoiding the spread of infected tubers, use of non-infested seed potato, application of organic amendments, solarisation, stubble burning, weed control, cleaning of farm machinery, and chemical and biological control (Franco, 1994; Jones et al., 2013). Biological control strategies using different organisms (such as bacteria, fungi and entomopathogenic nematodes) and other eco-compatible approaches (metabolites, essential oils, plant extracts, phytohormones and amendments), either alone or as part of a combined control strategy show good results to reduce the root damage (less galls) and the nematode reproduction (Lax et al., 2022). However, field evaluations need to be further developed.

Phytosanitary risk 

Due to its adaptive capacity to different environments and its wide host range, N. aberrans s.l. is a major threat if it were to be introduced into new regions or if new pathotypes/groups were to be introduced into new areas (Inserra et al., 2005; Lax et al., 2022).

Although N. aberrans s.l. distribution is restricted to the American continent, it has quarantine importance and is subject to international legislation to prevent its spread to other regions, such as the European Union. Detection in potato tubers is very important for regulatory and seed certification purposes. Post-entry quarantine procedures in the EPPO region are needed, together with equivalent checks before export to avoid the introduction of the South American potato pathotype/group. Only material for scientific purposes should normally be imported from South and North America. From other countries where N. aberrans s.l. is known to occur, the simplest practical measure is to restrict the introduction of soil, as such or accompanying plants (EPPO, 2021).

Anthoine G & Mugniéry D (2005) Variability of the ITS rDNA and identification of Nacobbus aberrans (Thorne, 1935) Thorne & Allen, 1944 (Nematoda: Pratylenchidae) by rDNA amplification. Nematology 7, 503-516.

Atkins SD, Manzanilla-López RH, Franco J, Peteira B & Kerry BR (2005) A molecular diagnostic method for detecting Nacobbus in soil and in potato tubers. Nematology 7, 193-202.

Canto-Saenz M, Arcos MJ, Jatala P, Haddad R (1996) Morphology, biology, and management of Nacobbus aberrans in Peru. Nematropica 26, 197.

Castiblanco O, Franco J & Montecinos R (1999) Razas y gama de hospedantes en diferentes poblaciones del nematodo Nacobbus aberrans (Thorne, 1935), Thorne & Allen 1944. Revista Latinoamericana de la Papa 11, 85-96.

Coolen WA (1979) Methods for the extraction of Meloidogyne spp. and other nematodes from roots and soil. In: Root-knot Nematodes (Meloidogyne species), Systematics, Biology and Control (Eds Lamberti F & Taylor CE), pp. 317–329. Academic Press, London (GB).

Corrales Arango A (2007) Dinámica poblacional del ‘nematodo del rosario de la raíz’ (Nacobbus aberrans) en las prácticas culturales del cultivo de tomate de mesa (Lycopersicum esculentum Mill) y pérdidas que causa. Ibarra-Imbabura (Degree Thesis). Universidad Técnica del Norte, Ibarra, Ecuador.

Costilla MA (1985a) El falso nematode del nudo Nacobbus aberrans (Thorne, 1935) Thorne & Allen, 1944 y su relación con el cultivo de papa en el Noroeste argentino. Revista Industrial y Agrícola de Tucumán 62, 79-97.

Costilla MA (1985b) Un método rápido para la extracción y observación de estados juveniles de Nacobbus aberrans en tubérculos de papa. Revista Industrial y Agrícola de Tucumán 62, 163-170.

Cristóbal AJ, Cid del Prado IV, Marbán-Mendoza N, Sánchez GP, Mora-Aguilera G & Manzanilla LRH (2001) Sobrevivencia de estadios biológicos de Nacobbus aberrans en condiciones de campo. Nematropica 31, 229-235.

Cristóbal-Alejo J, Mora-Aguilera G, Manzanilla-López RH, Marbán-Mendoza N, Sánchez-García P, Cid del Prado Vera I & Evans K (2006) Epidemiology and integrated control of Nacobbus aberrans on tomato in Mexico. Nematology 8, 727-737.

Doucet ME & Lax P (2005) El género Nacobbus Thorne & Allen, 1944 en Argentina. 6. La especie N. aberrans (Thorne, 1935) Thorne & Allen, 1944 (Nematoda: Tylenchida) y su relación con la agricultura. Anales de la Academia Nacional de Agronomía y Veterinaria 59, 5-45.

EFSA Panel on Plant Health (PLH), Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E et al. (2018) Pest categorisation of Nacobbus aberrans. EFSA Journal 16, e05249. https://doi.org/10.2903/j.efsa.2018.5249

EPPO (2009) EPPO Standards. Diagnostics. PM 7/5(2) Nacobbus aberrans sensu lato. EPPO Bulletin 39, 376-381.

EPPO (2021) EPPO Standards. Phytosanitary Procedures. PM 3/93 (1) Management of phytosanitary risks for potato crops resulting from movement of soil associated with root crops and potatoes. EPPO Bulletin 51, 418–435.

Franco J (1994) Problemas de nematodos en la producción de papa en climas templados en la región andina. Nematropica 24, 179-195.

Franco J, Ortuño N, Oros R & Main G (1996) Biology and management of Nacobbus aberrans on potato in Bolivia. Nematropica 26, 204.

Franco J & Main G (2008) Management of nematodes of Andean tuber and grain crops. In: Integrated Management and Biocontrol of Vegetable and Grain Crops Nematodes. Ciancio A, Mukerji KG (eds.). Springer, Dordrecht, Netherlands, 99-117.

Inserra RN, Di-Vito M & Ferris H (1984) Influence of Nacobbus aberrans densities on growth of sugarbeet and kochia in pots. Journal of Nematology 16, 393-395.

Inserra RN, Chitambar JJ, Chitwood DJ & Handoo ZA (2005) The potato pathotype of the false-root knot nematode, Nacobbus aberrans. A List of Exotic Nematode Plant Pests of Agricultural and Environmental Significance to the United States. University of Nebraska-Lincoln, Society of Nematologists, and USDA-APHIS.

Jatala P & Kaltenbach R (1979) Survival of Nacobbus aberrans in adverse conditions (Abstract). Journal of Nematology 11, 303.

Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG, Kikuchi T, Manzanilla‐López R, Palomares‐Rius JE, Wesemael WM, Perry RN (2013) Top 10 plant‐parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14, 946-961.

Lax P, Rondan Dueñas JC, Coronel NB, Gardenal CN, Bima P & Doucet ME (2011) Host range study of Argentine Nacobbus aberrans sensu Sher populations and comments on the differential host test. Crop Protection 30, 1414-1420.

Lax P, Tordable MC, Macagno J, Bima P & Doucet ME (2013) Response of different potato cultivars to the presence of Nacobbus aberrans. Nematropica 43, 83-90.

Lax P, Gonzalez-Ittig RE, Rondan Dueñas JC, Andrade AJ, Gardenal CN, Franco J & Doucet ME (2021) Decrypting species in the Nacobbus aberrans (Nematoda: Pratylenchidae) complex using integrative taxonomy. Zoologica Scripta 50, 667-688.

Lax P, Passone MA, Becerra AG, Sosa AL, Ciancio A, Finetti Sialer MM & Rosso LC (2022) Sustainable strategies for management of the ‘false root-knot nematode’ Nacobbus spp. Frontiers Plant Science 13, 1046315. https://doi.org/10.3389/fpls.2022.1046315

Manzanilla-López RH, Costilla MA, Doucet M, Inserra RN, Lehman PS, Cid del Prado-Vera I, Souza RM & Evans K (2002) The genus Nacobbus Thorne & Allen, 1944 (Nematoda: Pratylenchidae): systematics, distribution, biology and management. Nematropica 32, 149-227.

Ortuño N, Oros R, Main G & Franco J (1996) Detección de nematodos por el método de la bolsa cerrada. Serie Ficha Técnica 2/96.

Sher SA (1970) Revision of the genus Nacobbus Thorne and Allen, 1944 (Nematoda: Tylenchoidea). Journal of Nematology 2, 228-235.

This datasheet was extensively revised in 2023 by Paola Lax, Instituto de Diversidad y Ecología Animal (CONICET-UNC), Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina. Her valuable contribution is gratefully acknowledged.

EPPO (2024) Nacobbus aberrans sensu lato. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-05-09)

This datasheet was first published in the EPPO Bulletin in 1984 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1^st and 2^nd edition). CABI, Wallingford (GB).

EPPO (1984) Data sheets on quarantine organisms No. 144, Nacobbus aberrans. EPPO Bulletin 14(1), 61-66. https://doi.org/10.1111/j.1365-2338.1984.tb01983.x