Asian Citrus Root-knot | Pest Rating Proposals and Final Ratings

California Pest Rating for

Asian Citrus Root-knot Nematodes:

Meloidogyne citri Zhang, Gao & Weng, 1990;
donghaiensis Zheng, Lin & Zheng, 1990;
fujianensis Pan, 1985
indica Whitehead, 1968;
jianyangensis Yang, Hu, Chen & Zhu, 1990;
kongi Yang, Wang & Feng, 1988;
mingnanica Zhang, 1993

Pest Rating: A

PEST RATING PROFILE

Initiating Event:

A statewide survey of California’s major commercial citrus production sites was conducted in 2012-13 for the probable detection of member species that comprise the Asian citrus root-knot nematode (ACRKN) complex. The species are invasive and listed in the 2012 United States Department of Agriculture (USDA) CAPS Priority Pest List for survey. A permanent rating is proposed here for the complex of species and each individual member.

History & Status:

Background: The Asian citrus root-knot nematodes are a complex of species that in Asia attack the roots of Citrus spp. The species have not been found outside of China and India where the climate ranges from semi-tropical to temperate. Currently, there is a paucity of information on the biology and economic damage potential of each species, however, root-knot nematodes are known to economically damage crops and therefore ACRKN, if introduced to the United States, have the potential to negatively impact citrus production.

Life Cycle: The seven species comprising the complex of Asian citrus root-knot nematodes (Meloidogyne spp.) have life cycles and feeding behaviors similar to other root knot nematode species. Meloidogyne spp are sedentary endoparasites that feed 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. Very little is known about the biology of all ACRKN species. Pan et al., (1999) provided information on the biology of M. fujianensis on Citrus reticulata in Fujian Province, China. The species is active there throughout the year with peak infection occurring between September-October and March-April. During that time juveniles of various stages may be present in the soil. The life cycle of M. fujianensis is 55-60 days at 25° with 33-35 days from root penetration to egg production. M. indica took 28-35 days from root penetration to egg production on Satsuma, sour orange and tomato (Vovlas & Inserra, 2000).

Hosts: Citrus is the primary host for all ASRKN species. Experimental hosts include pepper and tomato as non-citrus hosts. Some of the nematode species show preferences to certain Citrus species over others. Meloidogyne citri: Citrus spp. (citrus), C. reticulata (mandarin/tangerine orange), C. unshiu (Satsuma orange), C. aurantium (sour orange), Solanum lycopersicum (tomato). M. donghaiensis: mandarin/tangerine orange. M. fujianensis: Imperata cylindrical (cogon grass), mandarin/tangerine orange. M. indica: citrus, C. aurantifolia (lime), C. sinensis (orange), Morinda officianalis (morinda). M. jianyangensis: citrus, mandarin/tangerine orange. M. kongi: citrus, Capsicum sp. (pepper). M. mingnanica: citrus, Satsuma citrus, Poncirus trifoliate (trifoliate or hardy orange), sour orange (as an experimental host) (Davis & Venette, 2004).

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 of host.

Damage Potential: The damage potential and economic impact of ACRKN is not well known. The impact of single species is difficult to determine as these nematodes usually occur in mixed populations. In China and India, estimated losses in citrus production to ACRKN infestation are 20-50% (Pan, 1985; Vovlas & Inserra, 2000). Information is sparse on the damage potential of individual members of the ACRKN group however, Meloidogyne spp. are known to be one of the most economically important plant parasitic nematodes attacking a wide range of crops worldwide and causes global economic losses that average 10-11%, although this figure is thought to be grossly underestimated.

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

Worldwide Distribution: Asia: China (Meloidogyne citri, M. donghaiensis, M. fujianensis, M. indica, M. jianyangensis, M. kongi, and M. mingnancia) and India (M. indica).

Official Control: Of the seven species belonging to ACRKN, Meloidogyne fujianensis and M. kongi are on Taiwan’s Harmful Organism List, and M. indica is on the similar list for Indonesia and Timor-Leste. M. citri and M. fujianensis are prevented into Florida through the movement of nursery stock and other plants and plant products (5B-3.0038: Quarantine Action, Department of Agriculture and consumer Services, division of Plant Industry).

California Distribution: ACRKN are not known to be present in California.

California Interceptions: ACRKN have never been detected in incoming shipments of plants and soil to California.

The risk Asian citrus root-knot nematodes 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). If introduced, it is likely that ACRKN is able to establish a widespread distribution in California. Meloidogyne citri, M. donghaiensis, M. fujianensis, M. indica, and M. mingnanica are favored by tropical and sub-tropical climates (Davis & Venette, 2004), while M. jianyangensis and M. kongi are more temperate climate species. Based on what is currently known about the geographical distribution of ASRKN species, Davis and Venette (2004) suggested that because of their climate preference, the first group of species may not find suitable climate in California, while M. jianyangensis may find suitable climate in California in the northern region extending along an eastern-southern strip to Kern County. However, their forecast is based on current known geographical distribution of the species and not of the associated hosts. Most citrus are adapted to warm, tropical or subtropical climates. There is always the possibility that California will support populations of the first group of species, especially as large acreages are under citrus, tomato and pepper production statewide.

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 Medium (2). ACRKN has a moderate host range of several Citrus species, tomato and pepper. However, citrus and tomato are major crops grown over extensive acreage within California.

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). ACRKN species have high reproduction and are easily spread to non-infected sites through the movement of infected plant roots, soil/planting media, contaminated cultivation equipment and irrigation water.

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).
D. The pest could negatively change normal 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). Introduction and establishment of ACRKN could lower crop yield, crop value, result in reduction or loss of market due to the imposition of quarantines against California, require costly changes in normal production cultural practices including restriction and delivery of irrigation water within and between fields.

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. The pest significantly impacts 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). Introduction and establishment of ACRKN species to urban and commercial ornamental sites could significantly impact gardening/cultural practices thereby triggering additional official or private treatments.

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 = 14 (High).

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: ACRKN are not established in California (0).

Final Score:

Final Score: Score of Consequences of Introduction – Score of Post Entry Distribution and Survey Information = 14 (High).

Uncertainty:

It is possible that the Asian citrus root-knot nematode 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, the likelihood that ACRKN species have already gained entry into California’s commercial citrus fields is minimal at best when the following is considered: ACRKN species were not detected by CDFA Nematology in statewide surveys of citrus, tomato and pepper commercial production sites in 2005-2008, and in citrus production sites in 2012-2013. Also, none of the species belonging to the complex have been detected in regulatory samples generated through CDFA’s nematode control and phytosanitary certification programs; ACRKN species have not been reported from California by other researchers/nematologists. The status of ACRKN species in non-cultivated and residential environments is not known. Those environments may serve as sources of inoculum for infestations of citrus commercial production sites. Identification to species level through DNA analysis is now essential for accurate identification of these species. Future detection of ACRKN species in California soils may result in alteration of their current proposed rating.

Conclusion and Rating Justification:

Based on the evidence presented above, the Asian citrus root knot nematodes, Meloidogyne spp., are pests of high risk to citrus production in California.

A permanent pest rating of “A” is proposed for each Asian citrus root-knot nematode species, namely, Meloidogyne citri, M. donghaiensis, M. fujianensis, M. indica, M. jianyagensis, M. kongi and M. mingnanica.

References:

CABI. 2014. Crop Protection Compendium. www.cabi.org/cpc/ .

Davis, E. E. and R. C. Venette. 2004. Mini risk assessment Asian Citrus Root-knot Nematodes: Meloidogyne citri Zhang, Gao & Weng; M. donghaiensis Zheng, Lin & Zheng; M. fujianensis Pan; M. indica Whitehead; M. jianyangensis Yang, Hu, Chen & Zhu; M. kongi Yang, Wang and Feng; and M. mingnanica Zhang [Nematoda: Meloidogynidae]. CAPS PRA. http://www.aphis.usda.gov/plant_health/plant_pest_info/pest_detection/downloads/pra/asiancitrusmmeloidogynepra.pdf .

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

Pan, C. S. 1985. Studies on plant-parasitic nematodes on economically important crops in Fujian III. Description of Meloidogyne fujianensis n. sp. (Nematode: Meloidogynidae) infesting Citrus in Nanjing County. Acta Zoologica Sinica 31:263-268.

Pan, C., X. Hu and J. Lin. 1999. Temporal fluctuations in Meloidogyne fujianensis parasitizing Citrus reticulata in Nanjing, China. Nematologia Mediterranea 27: 327-330.

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

Vovlas, N. and R. N. Inserra. 2000. Root-knot nematodes as parasites of Citrus. Proceedings of the International Society of Citriculture, Vol. II 2:812-817.

Responsible Party:

Dr. John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-262-1110, plant.health[@]cdfa.ca.gov.