Meloidogyne enterolobii Yang and Eisenback, 1983.

California Pest Rating for

Meloidogyne enterolobii Yang and Eisenback, 1983.

(A Root knot Nematode)

Pest Rating: A

PEST RATING PROFILE*

*Revised June 25, 2019

Initiating Event:

None.

History & Status:

Background: Meloidogyne enterolobii is considered one of the most important root-knot nematode species because of its ability to overcome resistance in important crops carrying genes of resistance to the main Meloidogyne spp. thereby causing substantial reduction in crop yields.

Meloidogyne enterolobii was first discovered parasitizing roots of pacara earpod tree, Enterolobium contortisiliquum in China in 1983 (Yang & Eisenback, 1983). The nematode species was later described from other regions in China and mainly on guava, Psidium guajava. Taxonomically, M. enterolobii is a senior synonym of M. mayaguensis that was originally described from Puerto Rico parasitizing aubergine (Solanum melongena) roots (Xu et al., 2004; Tigano et al., 2010). Meloidogyne enterolobii belongs to the family Meloidogynidae in the order Tylenchida.

Life Cycle: Meloidogyne enterolobii is a root knot nematode species with a life cycle and feeding behavior similar to other root knot nematode species. It is a sedentary endoparasite that feeds within host plant roots. Adult females embedded in host roots produce eggs within a mass either on the surface of, or within roots. The first stage juvenile develops within the egg and molts to develop into the second stage. The second-stage juveniles (J2) are the infective stage that hatch from eggs, migrate in rhizosphere soil to host roots, reinfest the roots or are attracted to other nearby host roots which are then penetrated. Within roots, J2 establish a specialized feeding site or giant plant cells that are formed at the head end of the nematode in response to its feeding. The second stage juveniles become sedentary while feeding at the specialized site, increase in size and undergo two more molts and non-feeding stages before developing into mature adult females or males and completing the life cycle. Reproduction is by mitotic parthenogenesis. Generally, the life cycle for root knot nematodes may take about 30 days at 25-28°C and longer at lower temperatures.

Hosts: Major hosts include Capsicum annuum (pepper), Citrullus lanatus (watermelon), Coffeae arabica (coffee),Glycine max (soybean), Ipomoea batatas (sweet potato), Nicotiana tabacum (tobacco), Psidium guajava (guava),Solanum lycopersicum (tomato), S. melongena (eggplant), Gossypium sp. (cotton), Capsicum annuum (bell pepper), Apium graveolens (celery), Brassica oleracea var. oleracea (cabbage), Phaseolus vulgaris (common bean), (garden beet), (mustard), squash (all types), (sweet basil). Other minor hosts include Angelonia angustifolia, Aquilaria malaccensis, Brugmansia, Enterolobium contortisiliquum, Euphorbia punicea, Hibiscus, Maranta arundinacea, Morinda citrifolia, Morus nigra, Ocimum basilicum, Paulownia elongata, Syzygium aromaticum, Thunbergia, Tibouchina, Solanum tuberosum (potato), Bidens pilosa, Lactuca sativa (lettuce), and Cucumis sativus(cucumber) (CABI, 2014; EPPO, 2014, Paes-Takahashi et al. 2015, Overstreet et al., 2018). Several weed plants have also been reported as hosts for the guava root-knot nematode: American black nightshade, Bristly hawkbit, Bull nettle, Common purslane, Dichondra, Ground cherry, Hairy beggarticks, Hairy crabweed, Pokeweed, Purple nutsedge, Redroot pigweed, Sicklepod, Smooth pigweed, Spiny amaranth, three-lobed morning glory, Wild, mustard, Wild, poinsettia, and Yellow nutsedge (Overstreet et al., 2018)

Symptoms: Galls are produced on the roots of infected galls. Galls may occur singly or coalesce to form compounded root swellings. Above ground symptoms are general and typical of an impaired root system caused by biotic or abiotic factors. Visible symptoms of infection usually include unthriftiness, yellowing of leaves, wilting, defoliation, reduced growth and even death in three years.

Damage Potential: Populations of Meloidogyne enterolobii are able to overcome resistance in tomato cv. Rossol, soybean cv. Forrest, and sweet potato cv. CDH in West Africa. Damage to coffee has been observed in Cuba where the nematode is able to reproduce on resistant tomato varieties with the Mi 1.2 gene. The species may occur with, and is considered more damaging than the commonly distributed species, M. incognita, M. arenaria and M. javanica (Brito et al., 2002; CABI, 2014). Severe damage to guava (stunted growth, reduced leaf size, and reduced yield) has been observed in South Africa and Brazil (CABI, 2014; Carneiro et al., 2001).

Movement and Dispersal: Infected roots, bare root propagative material, and soil debris,

Worldwide Distribution: M. enterolobiiwas first reported from China (Yang & Eisenback, 1983). Since then it has been reported from Asia: Vietnam; Africa: Burkina Faso, Congo (Democratic Republic), Cote d’Ivoire, Malawi, Senegal, South Africa, Togo; South America: Brazil, Venezuela; Central America and Caribbean: Cuba, Guadeloupe, Guatemala, Martinique, Puerto Rico, Trinidad, Tobago; North America: Mexico, USA (Florida, North Carolina, South Carolina, Louisiana);Europe: Switzerland (Brito et al., 2004; CABI, 2014; EPPO, 2014; Ramírez-Suárez et al., 2014; Ye et al., 2013, Overstreet et al., 2018; Rutter et al., 2019).

Official Control: Meloidogyne enterolobii is on the A2 list for EPPO since 2010, and on the Alert list for NAPPO since 2002 (EPPO, 2014). Currently, it is on the Harmful Organism list for Costa Rica and the Republic of Korea (PCIT-APHIS, 2014). In the USA, Meloidogyne enterolobii is on the quarantine list of nematodes in Florida, andMississippi (National Plant Board, 2019). In North Carolina there is an internal quarantine (Wilson, 2018).

California Distribution: Meloidogyne enterolobii is not known to be present in California.

California Interceptions: There are no records of the detection of Meloidogyne enterolobii in incoming shipments of plants and soil to California.

The risk Meloidogyne enterlobii would pose to California is evaluated below.

Consequences of Introduction:

1) Climate/Host Interaction: Evaluate if the pest would have suitable hosts and climate to establish in California. Score:

-Low (1) not likely to establish in California; or likely to establish in very limited areas

-Medium (2) may be able to establish in a larger but limited part of California

– High (3) likely to establish a widespread distribution in California.

Risk is High (3). California has suitable climate and hosts for M. enterolobii. If introduced, the species is likely to establish a widespread distribution.

2) Known Pest Host Range: Evaluate the host range of the pest:

-Low (1) has a very limited host range

-Medium (2) has a moderate host range

– High (3) has a wide host range.

Risk is High (3). M. enterolobii has a wide and diverse host range.

3) Pest Dispersal Potential: Evaluate the dispersal potential of the pest:

-Low (1) does not have high reproductive or dispersal potential

-Medium (2) has either high reproductive or dispersal potential

– High (3) has both high reproduction and dispersal potential.

Risk is High (3). M. enterolobii has high reproduction. A single female M. enterolobii may produce several hundreds to over one thousand eggs in an egg mass, similar to other Meloidogyne species. Dispersal is mainly passive through the movement of infected roots and soils. The potential for spread is high.

4) Economic Impact: Evaluate the economic impact of the pest to California using these criteria:

A. The pest could lower crop yield.

B. The pest could lower crop value (includes increasing crop production costs).

C. The pest could trigger the loss of markets (includes quarantines by other states or countries).

D. The pest could negatively change normal production cultural practices.

E. The pest can vector, or is vectored, by another pestiferous organism.

F. The organism is injurious or poisonous to agriculturally important animals.

G. The organism can interfere with the delivery or supply of water for agricultural uses.

-Low (1) causes 0 or 1 of these impacts

-Medium (2) causes 2 of these impacts

– High (3) causes 3 or more of these impacts.

Risk is High (3). M. enterolobii is able to break resistance in important crops carrying genes of resistance to the main Meloidogyne spp. thereby causing substantial reduction in crop yields, crop value, loss of markets, including the likely imposition of quarantines by other states and countries against California. Pest management strategies may adversely affect normal cultural practices.

5) Environmental Impact: Evaluate the environmental impact of the pest on California using these criteria:

A. The pest could have a significant environmental impact such as lowering biodiversity, disrupting natural communities, or changing ecosystem processes.

B. The pest could directly affect threatened or endangered species.

C. The pest could impact threatened or endangered species by disrupting critical habitats.

D. The pest could trigger additional official or private treatment programs.

E. Significantly impacting cultural practices, home/urban gardening or ornamental plantings.

Score the pest for Environmental Impact:

– Low (1) causes none of the above to occur

– Medium (2) causes one of the above to occur

– High (3) causes two or more of the above to occur.

Risk is High (3). Several ornamental and perennial shrub plants are probable hosts of the nematode species. Infestations of M. enterolobii may lower biodiversity and disrupt natural plant communities, endanger critical habitats. Home gardening and ornamental plantings may also be impacted.

Consequences of Introduction to California for Common Name: Score

Add up the total score and include it here. (Score)

Low = 5-8 points

Medium = 9-12 points

High = 13-15 points

Total points obtained on evaluation of consequences of introduction to California = 15.

6) Post Entry Distribution and Survey Information: Evaluate the known distribution in California. Only official records identified by a taxonomic expert and supported by voucher specimens deposited in natural history collections should be considered. Pest incursions that have been eradicated, are under eradication, or have been delimited with no further detections should not be included. (Score)

–Not established (0) Pest never detected in California, or known only from incursions.

-Low (-1) Pest has a localized distribution in California, or is established in one suitable climate/host area (region).

-Medium (-2) Pest is widespread in California but not fully established in the endangered area, or pest established in two contiguous suitable climate/host areas.

-High (-3) Pest has fully established in the endangered area, or pest is reported in more than two contiguous or non-contiguous suitable climate/host areas

Evaluation is Not established (0).

Final Score:

Final Score: Score of Consequences of Introduction – Score of Post Entry Distribution and Survey Information = 15.

Uncertainty:

It is possible that the nematodes species may have entered the State undetected prior to 2005. This is largely due to the fact that prior to 2005 Meloidogyne spp. were not always identified, at the CDFA Nematology Laboratory, to species level when detected in samples that originated outside and within California. However, since 2005, M. enterolobii has never been detected in regulatory samples generated through CDFA’s nematode control and phytosanitary certification programs or through statewide nematode surveys of host plants grown in agricultural production sites and nurseries in California. Also, M. enterolobii has not been reported from California by other researchers/nematologists. The status of M. enterolobii in non-cultivated and residential environments is not known. Those environments may serve as sources of inoculum for infestations of cultivated production sites. Identification to species level through DNA analysis is now essential for accurate identification of this species. Future detection of the species in California soils may result in alteration of its current proposed rating.

Conclusion and Rating Justification:

Based on the evidence above the proposed rating for Meloidogyne enterlobii is A.

References:

Brito, J. A., Stanley, J., Cetintas, R., Powers, T., Inserra, R., McAvoy, G., Mendes, M.L., Crow, B., and Dickson, D. 2004. Identification and host preference of Meloidogyne mayaguensis and other root-knot nematodes from Florida, and their susceptibility to Pasteuria penetrans. Journal of Nematology 36:308-309.

CABI. 2014. Meloidogyne mayaguensis full datasheet. Crop Protection Compendium. www.cabi.org/cpc/.

EPPO. 2014. Meloidogyne enterolobii (MELGMY). PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://newpqr.eppo.int .

Han, H., Brito, J.A., and Dickson, D.W. 2012. First report of Meloidogyne enterolobii infecting Euphorbia puniceain Florida. Plant Disease 96 (11), p 1706.

Overstreet, C., McGawley, E.C., Clark, C., Rezende, J., Smith, T., and Sistrunk, M. 2018. Guava root knot nematode a potentially serious new pest in Louisiana. LSU Ag Center publication. https://msfb.org/wp-content/uploads/2018/11/guava-root-knot-nematode-adapdf.pdf

Paes-Takahashi, V. S., Soares, P. L. M., Carneiro, F. A., Ferreira, R. J., de Almeida, E. J., and dos Santos, J. M. 2015. Detection of Meloidogyne enterolobii in mulberry seedlings (Morus nigra L.). Ciência Rural 45(5):757-759. http://dx.doi.org/10.1590/0103-8478cr20130350.

Ramírez-Suárez, A., Rosas-Hernández, l., Alcasio-Rangel, S., Pérez Valenzuela, G., and Powers, T.O. 2014. First report of the root-knot Meloidogyne enterolobii parasitizing watermelon from Veracruz, Mexico. Plant Disease, 98:428.3.

Rutter, W. B., Skantar, A. M., Handoo, Z. A., Mueller, J. D., Aultman, S.P., and Agudelo, P. 2019. Meloidogyne enterolobii found infecting root-knot nematode resistant sweetpotato in South Carolina, United States. Plant Disease 103:4

Tigano, M., de Siqueira, K., Castagnone-Sereno, P., Mulet, K., Queiroz, P., Dos Santos, M., Teixeira, C., Almeida, M., Silva, J., and Carneiro, R. 2010. Genetic diversity of the root-knot Meloidogyne enterolobii and development of a SCAR marker for this guava-damaging species. Plant Pathology 59:1054-1061.

USDA PCIT. 2014. USDA Phytosanitary Certificate Issuance and Tracking System. Phytosanitary Export Database. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp .

Wilson, P. 2018. NCDA&CS declares an internal quarantine for all North Carolina counties for the Guava knot nematode. http://www.ncagr.gov/paffairs/release/2018/10-18guavarootknotnematode.htm

Xu, J., Liu, P., Meng, Q., and Long, H. 2004. Characterization of Meloidogyne species from China using isozyme, phenotypes and amplified mitochondrial DNA restriction fragment length polymorphism. European Journal of Plant Pathology 110:309–15.

Yang, B., and Eisenback, J. D. 1983. Meloidogyne enterolobii n. sp. (Meloidogynidae), a root-knot nematode parasitizing pacara earpod tree in China. Journal of Nematology 15:381–91.

Ye, W., Koenning, M, S. R., Zhuo, K. and Liao, J. L. 2013. First report of Meloidogyne enterolobii on cotton and soybean in North Carolina, United States. Plant Disease 97(9), p 1262.

Responsible Party:

John J. Chitambar, and Heather J. Scheck, Former and Current Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, plant.health[@]cdfa.ca.gov.

Comment Period: CLOSED

The 45-day comment period opened on Aug 3, 2016 and closed on Sep 17, 2016.

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