Anguina tritici (Steinbach, 1799), Chitwood, 1935

California Pest Rating for

Wheat Seed gall nematode

Tylenchida: Anguinidae

Pest Rating: A

PEST RATING PROFILE

Initiating Event:

A pest risk assessment of Anguina tritici and a re-evaluation of its current pest rating in California is presented here.

History & Status:

Background: Anguina tritici, commonly named the wheat seed gall nematode, was the first plant-parasitic nematodes to be described in literature. The wheat seed gall nematode is an economically important pest of wheat (Triticum sp.) and rye (Secale cereal L.), causing a disease called ‘ear-cockle’ or seed gall, that has destroyed 30-70% of the wheat crop in undeveloped parts of the world (Clark et. al. 1991, Ferris, 2013, Subbotin & Riley, 2012). This nematode was first found in the United States in 1909 and subsequently in numerous states, primarily in wheat but also in rye to a lesser extent (PERAL, 2015). Modern mechanized agricultural seed grading practices that result in separation of clean seed from galls, along with crop rotation, have practically eliminated A. tritici from countries which have adopted these practices, and the nematode has not been found in the United States since 1975 (PERAL, 2015). Furthermore, from 2005 to 2009, CDFA conducted USDA CAPS sponsored statewide surveys for A. tritici and 21 other target nematode species associated with major host plant species, including wheat, barley, and several other agricultural crops and ornamentals in California’s major cropping and nursery production regions. Anguina tritici was not detected (Chitambar et al., 2008). However, A. tritici is still a problem in traditional farming systems in west and south Asia where modern mechanized seed grading practices are not widely adapted or efficiently applied (SON, 2003).

Hosts: Emmer (Triticum monococcum), rye (Secale cereale), spelt (T. spelta), and bread wheat (T. aestivum) are the primary hosts. Barley (Hordeum vulgare), oats (Avena sativa), durum wheat (T. durum), and rivet wheat (T. turgidum) are minor hosts (CABI, 2016; EPPO, 2016; Mackesy & Sullivan, 2016).

Symptoms: Anguina tritici infect aboveground plant parts by invading and becoming endoparasitic in the plant tissue (Clark et al., 1991). Slight elevations occur on upper leaf surface with indentations on the lower side. Other symptoms include wrinkling, twisting, curling of the margins towards the midrib, distortion, buckling, swelling and bulging (CABI, 2016). Infected plants become stunted and have shorter and deformed stems and leaves (Subbotin & Riley, 2012). In severe infection, plants do not form ears or form only stunted ears on stunted stems. Generally infested ears are smaller, shorter and thicker than healthy ones, and have abnormally spreading glumes. Some or all grains are transformed to galls which are light to dark brown to black, hard to the touch and filled with numerous infective juvenile nematodes. (Subbotin & Riley, 2012). The entire above ground plant is distorted to some degree and a disease problem is usually obvious (CABI, 2016). Wheat seeds with low nematode numbers do not show typical symptoms of infection, i.e., seed galls (Lal & Lal, 2006).

Disease Development: Anguina tritici prefers cool conditions in most climates where wheat is grown. The favored micro-habitat for the survival of A. tritici is within seed galls, where all stages are protected from hostile environmental factors. This nematode also survives on the soil surface, either in or out of galls, and in dry seed storage (CABI, 2016). Second stage juveniles (J2s) within drying galls are capable of entering a cryptobiotic state to survive during dry conditions (Bird and Buttrose, 1974). Viable juveniles have been recovered for up to periods as long as 38 years (Ferris, 2013). In moist soils, galls are softened enough to release infective second stage juveniles. The juveniles enter young seedlings and move upwards within the plant to the meristem or concentrate in the leaf axis of shoots where they feed ectoparasitically and remain there until inflorescence develops. Juveniles invade the floral tissue and gall formation is stimulated. Juveniles develop into 40 or more adult males or females with each female laying 30,000 or more eggs and/or juveniles (CABI, 2016; Subbotin & Riley, 2012). Swarup and Sosa-Moss (1990) reported that a minimum population of 10,000 juveniles/kg soil is needed for the development of ear-cockle disease and the severity of the disease is greatest when nematode galls are place in soil at a depth of 2-6 cm than when placed deeper.

Transmission: The principal means of dispersion is by wheat seed containing infected galls in commerce and by sowing infected galls in fields. Other means of spread include straw from an infected crop, rainfall and flooding, natural migration and cow, sheep, sparrow, pigeon and goldfinch manure. A. tritici is also spread by animal feet, farm implements and machines, and by wind (Leukel, 1957).

Worldwide Distribution: Anguina tritici has been reported in Africa: Egypt and Ethiopia. Asia: Afghanistan, China, India, Iran, Iraq, Israel, Pakistan, Saudi Arabia, South Korea, Syria, Slovenia, and Taiwan. Europe: Austria, Azerbaijan, Bulgaria, Croatia, Cyprus, France, Germany, Greece, Hungary, Ireland, Italy, Lithuania, Netherlands, Poland, Romania, Russia, Serbia, Spain, Sweden, Switzerland, Turkey, Ukraine, and the United Kingdom (UK). Oceania: Australia and New Zealand (CABI, 2017).

Official Control: Anguina tritici is in the ‘Harmful organism Lists’ for Argentina, Brazil, Chile, Colombia, Ecuador, Egypt, Guatemala, Indonesia, Israel, Madagascar, Namibia, Nepal, New Zealand, Paraguay, Peru, South Africa, Taiwan, Thailand, Timor-Leste, and Uruguay (USDA-PCIT, 2017).

California Distribution: Anguina tritici is not present in California.

US Distribution: Although formerly present in several states, Anguina tritici was eliminated in 1975 and is not present in the U.S.

California Interceptions: Anguina tritici has never been intercepted in California (CDFA Pest and Damage Reports Database).

While the likelihood of introduction of Anguina tritici into California is minimal largely due to effective ongoing modern seed grading and other practices, the economic damage potential of this pest cannot be undermined. As stated earlier, wheat seeds infested with low populations of the nematode may not show typical symptoms of seed galling and pose the probability of accidental introductions. Therefore, the risk Anguina tritici (Wheat seed gall nematode) would pose to California, consequent to its introduction, is evaluated below:

Consequences of Introduction:

1) Climate/Host Interaction: Wheat, the main host of Anguina tritici, is primarily grown in Sacramento Valley, San Joaquin Valley, and Central Valley regions, and Imperial County (USDA-NASS Wheat County Estimates 2008). If introduced into California, Anguina tritici is likely to establish wherever wheat is grown within the state. Therefore, it receives a High (3) score in this category.

Evaluate if the pest would have suitable hosts and climate to establish in California:

Score: 3

– 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.

2) Known Pest Host Range: Primary hosts of Anguina tritici include wheat, rye, spelt and emmer wheat Oats, barley, durum wheat and rivet wheat are considered minor hosts. It receives a Medium (2) score in this category.

Evaluate the host range of the pest:

Score: 2

– Low (1) has a very limited host range.

– Medium (2) has a moderate host range.

– High (3) has a wide host range.

3) Pest Dispersal Potential: Reproduction of Anguina tritici is amphimictic. Mating occurs and female produces up to 2000 eggs per individual over several weeks. These eggs hatch and produce juvenile two stage (J2s), which remain within the galls as the survival stage and perpetuate plant infection as the invasive stage in following years. Dry galls are harvested with developed seeds, and each gall may contain thousands of J2s (Crop Protection Compendium). Anguina tritici produces one generation per year (Ferris, 2013). It is likely to enter California through transport of infested host plants or seed material. Since 2006, the import of Triticum sp. seed and Secale sp. is allowed from certain countries, some of which are known to have tritici (USDA- 2015). Because of its high reproduction and dispersal potential, Anguina tritici receives a High (3) score in this category.

Evaluate the natural and artificial dispersal potential of the pest:

Score: 3

– 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.

4) Economic Impact: Anguina tritici can cause severe crop losses to wheat 70% and rye (35-65%) in underdeveloped and developing countries due to poor agricultural practices, monoculture and use of poor quality seed. While there may be insignificant damage to California grown wheat and rye by this nematode due to modern agricultural production systems, export of CA grown grains to international markets can be severely hampered due to historical records of the presence of this nematode in production areas of the state (SON, 2003). The interaction of this nematode and Rathayibacter tritici in wheat in India results in an oozing bacterial infection of the grain known as ‘Tundu’ disease. The disease is also known as spike blight or yellow ear rot. (Ferris, 2013). Dilohosphora alopecuri in association with Anguina tritici could result in Dilophosphorosis disease of wheat where the spike is covered by black sticky mass. It receives a High (3) score in this category.

Evaluate the economic impact of the pest to California using the criteria below:

Economic Impact: A, B, C, E

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.

Economic Impact Score: 3

– 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.

5) Environmental Impact: Anguina tritici infestation is likely to cause ear-cockle disease in Sacramento/San Joaquin area and central valley. To prevent ear-cockle and spread of this nematode species, growers would require seed cleaning and crop rotation to eliminate the pest. Hot water treatments would be needed to eradicate A. tritici from seed lots and mechanical separation of wheat seeds from nematode galls. (PKB 2016). Additionally, infestations of tritici could significantly impact irrigation and other cultural practices. Therefore, it receives a High (3) score in this category.

Evaluate the environmental impact of the pest on California using the criteria below:

Environmental Impact: D, E

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:

Environmental Impact Score: 3

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

– Medium (2) causes 2 of these impacts.

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

**Consequences of Introduction to California for Anguina tritici (Wheat seed gall Nematode): High (14)**

Add up the total score and include it here:

-Low = 5-8 points

-Medium = 9-12 points

–High = 13-15 points

6) Post Entry Distribution and Survey Information: Anguina tritici has never been found in the environment and receives a Not established (0) in this category.

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: 0

–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.

Final Score:

The final score is the consequences of introduction score minus the post entry distribution and survey information score: High (14)

Uncertainty:

Anguina tritici has never been detected through regulatory pathways in California. Introduction of the nematode species into California can still occur especially in seeds that pass inspection because they may be infested with low numbers of nematode inoculum and not transformed to typical galls. Inspection of wheat fields for symptomatic plants and commercial seed lots in storage or moved in trade is necessary to further confirm the non-presence status of Anguina triticii in California.

Conclusion and Rating Justification:

Based on all the evidence presented above, Anguina tritici would likely have significant economic and environmental impacts if it were to enter and establish in Wheat growing areas of California. Therefore, an “A” rating is justified and proposed herein.

References:

Bird, A. F., and M. S. Buttrose. 1974. Ultrastructural changes in the nematode Anguina tritici associated with anhydrobiosis. Journal of Ultrastructure Research 48: 177-189.
Clark, R.A., R. P. Esser, and J. H. O’Bannon. 1991. Procedures to detect wheat seed gall nematode in Florida. Nematology Circular No. 186. Florida Dept. of Agric. & Consumer Services, Division of Plant Industry
CABI 2016. Anguina tritici (wheat seed gall nematode) datasheet (full). http://www.cabi.org/cpc/
Chitambar, J., K. Dong, S. Subbotin, and R. Luna. California Statewide Nematode Survey Project. California Plant Pest and Disease Report, 24: 59
2016. Anguina tritici (ANGUTR). PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://newpqr.eppo.int
Ferris, H. 2013. Nemaplex: The Nematode Plant Expert Information System: A Virtual Encyclopedia on Soil and Plant Nematodes: Anguina tritici. University of California, Davis. December 7, 2016 http://plpnemweb.ucdavis.edu/nemaplex/Taxadata/G006S4.htm
Lal, R., and A. Lal. Plant parasitic nematode intercepted ffrom seeds, soil clods and packing material under import quarantine. Journal of New Seeds. *: 49-60.
Leukel, R. W., 1957. Nematode Disease of wheat and rye. USDA Farmers Bulletin, 1607.
Mackesy, D. Z., and M. Sullivan. CPHST Pest datasheet for Anguina tritici. USDA-APHISPPQ-CPHST. download.ceris.purdue.edu/file/3293
2015. Qualitative pest risk analysis for the wheat gall nematode, Anguina tritici, in U.S. United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, Center for Plant Health Science and Technology, Plant Epidemiology and Risk Analysis Laboratory.
Pest and Damage Report Database: Plant Health and Pest Prevention Services, California Department of Food and Agriculture. December 5, 2016 http://phpps.cdfa.ca.gov/user/frmLogon2.asp
PKB 2016. Plantwise Technical Fact Sheet: Wheat Seed Gall Nematode. Plantwise Knowledge Bank. http://www.plantwise.org/KnowledgeBank/Datasheet.aspx?dsid=5388
2003 Exotic Nematode Plant Pests of Agricultural and Environmental Significance to United States, The Society of Nematologists. Anguina tritici
Subbotin, S. A., and I. T. Riley. Stem and gall nematodes. In Practical Plant Nematology (book) Edited by R. H. Manzanilla-Lopez and N. Marbán-Mendoza. Biblioteca Basica de Agricultura, p. 521-577.
Swarup, G., and C. Sosa-Moss. Nematode parasites of cereals. In Plant Parasitic Neamtodes in Subtropical and Tropical Agriculture, edited by M. Luc, R. A. Sikora, and J. Bridge. 109-136.
2015. Plants for planting manual. Interim edition, updated 12/23/2015. https://www.aphis.usda.gov/import_export/plants/manuals/ports/downloads/plants_for_planting.pdf.
USDA NASS: 2008 California Wheat County Estimates https://www.nass.usda.gov/Statistics_by_State/California/Publications/County_Estimates/2009/200902whetf.pdf
USDA Phytosanitary Certificate Issuance & Tracking System (PCIT): Phytosanitary Export Database (PExD), December 5, 2016 https://pcit.aphis.usda.gov/PExD/faces/PExDReport.jsp

Responsible Party:

Raj Randhawa, Senior Environmental Scientist; 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.

Comment Period: CLOSED

3/3/2017 – 4/17/2017

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