Anguina funesta Price, Fisher & Kerr, 1979

California Pest Rating for
Anguina funesta Price, Fisher & Kerr, 1979
Pest Rating: A 


Initiating Event:


History & Status:

Background:  Anguina funesta is a plant parasitic nematode that induces formation of galls in developing seeds of annual rye grass (Lolium rigidium), Festuca and Vulpia species.  Commonly known as a seed gall nematode, A. funesta is not only an agricultural pest of economic significance in its own right, but is considered more important because it is a vector of the toxigenic actinomycete bacterium, Rathyibacter toxicus that causes Rathayibacter poisoning most commonly known as annual ryegrass toxicity (ARGT) disease (Murray et al., 2014; Riley & Barbetti, 2008)This bacterium is also vectored by other Anguina species, namely, A. agrostis, A. tritici, A. australis, and A. paludicola, and is a USDA APHIS Select Agent (Murray et al., 2014).  It is also noteworthy that Anguina funesta and other Anguina species are vectors of the fungus, Dilophospora alopecuri which inhibits gall formation and bacterial colonization thereby providing biological control of both nematode and bacterium.  Rathyibacter toxicus and Dilophospora alopecuri are transported to the plant host by adhering to the external cuticular surface of A. funesta.

The first record of ARGT was in Southern Australia in 1956, and caused considerable crop and animal losses.   Since then, ARGT and A. funesta spread to Western Australia, South Africa in 1981, and Japan in 1997, most likely with the importation of contaminated ryegrass seed and hay from Australia (Meng et al., 2012).  Both nematode and bacterial pathogen now continue to be an economic problem in northern cropping regions of Western Australia.  They generally follow a pattern of increase, impact, and then decline.  The decline appears to be associated with the build-up of Dilophosphora alopecuri and alterations in land management practices that had supported high host densities protected through to seed set (Subbotin & Riley, 2012).

In the USA, Anguina funesta has only been reported from Oregon having been detected in annual ryegrass seed lots in 2010.  Rathayibacter toxicus was not found in Oregon (ODA, 2011; Meng et al., 2012).  To date, the nematode and bacterial species have not been reported from any other US states outside of Oregon.  Anguina funesta has not been detected in California, nor was it found in turf and pasture seed samples analyzed at CDFA in 2012.  During that year, the CDFA Nematology Laboratory did not detect seed gall nematodes in seed samples of perennial ryegrass, tall fescue, and annual bluegrass received from various sources in Oregon, California, and Arizona and maintained in storage at the CDFA Seed Laboratory.

Hosts:  The principal host of A. funesta is annual ryegrass (Lolium rigidum).  It also induces galls in Festuca and Vulpia species.  Only L. rigidum and V. myuros are natural hosts of the nematode pathogen (Subbotin & Riley, 2012).

Symptoms:  Ryegrass plants do not show any visible symptoms of infection until inflorescence appears.  Nematode galls in annual ryegrass are difficult detect in the field as galls are covered by lemma and paleas.  However, once the latter are removed the galls are shrunken, fusiform, smaller than normal seed, and purplish.  On the other hand, the bacterial pathogen, R. toxicus may remain within a nematode gall or ooze out and partly or completely cover a gall with yellow bacterial slime which turns orange once it dries.  Also, while infected plants do not exhibit apparent symptoms, some entire seed heads may be twisted and malformed and covered with yellow slime.  However, the absence of slime (gummosis) does not necessarily indicate that a field is free of the bacterium (Murray et al., 2014; Putnam, 2011).

Disease cycle: Mature seed galls induced in the plant by the nematode contain anhydrobiotic second stage juveniles (J2) which form its survival and dispersal stage.  These juveniles overwinter in seed galls on the soil surface and can survive in dry state for many years.  Under moist conditions, the nematodes rehydrate, become active, and emerge from degrading galls onto the soil surface.  If the soil surface dries out, then the juveniles again become anhydrobiotic until another period of rehydration.   In moist soil surfaces, active juveniles seek and invade host seedlings and feed on the growing point (meristem tissue) of tillers where they accumulate until ovaries initiate development.  Then they invade ovaries of inflorescence and transform developing seed into seed galls.  J2 feed within galls, and develop through two further juveniles stages into adults.  A gall may be infested with a few to 20 male and female nematodes.  Sexual reproduction is necessary for formation of successive generations and occurs within the galls resulting in several hundred eggs per gall.  J2s hatch from the eggs within galls. Freshly-hatched J2s cannot survive desiccation, however, as infested plants mature and senesce, J2s also mature into their anhydrobiotic survival stage.  Galls are harvested and replanted along with healthy seed.  During harvest, galls fall to the ground and remain there until the nematodes regain activity under moist spring conditions, thus completing the cycle.  Toxigenic Rathyibacter toxicus bacteria in soil adhere to the external cuticular surface of Anguina J2s and are carried into the host plant’s inflorescence and nematode galls where thy proliferate and colonize these structures.  As the plant matures, bacteria produce glycolipid toxins known as corynetoxins that when consumed, cause neurological disorders, toxicosis, and fatality in animals.  When galls fall to the ground at harvest, bacteria reenter the soil (Riley & Barbetti, 2008; Subbotin & Riley, 2012).

Spread:  The nematode and bacteria can be spread commonly in galls intermixed with non-cleaned or poorly cleaned grass seed lots.  They can be dispersed by wind and in hay.  Other means of spread include infested soil/gall contaminated machinery, vehicles, humans and animals or run-off water.

Damage Potential:   While Anguina funesta will reduce healthy seed set in host plants, it must be noted that galled florets are likely to be removed with regular seed cleaning procedures.  However, there is the possibility for A. funesta galls to be accidently overlooked during cleaning procedures because they are concealed by lemma and palea coverings.  In which case, the likelihood of introduction to non-infested regions is increased.  The nematode species is considered a “High-Risk” species by USDA and the Society of Nematologists (SON, not dated), mainly due to its ability to vector the toxigenic bacterium which is a USDA APHIS Select Agent.  The threat of introduction, spread and establishment of the bacterium is very high due to the presence of susceptible grasses and the occurrence of Anguina species in the USA including California.  Pasture, rangeland, private and commercial lawns and turf gardens cultivated to annual ryegrass and fescue grasses are potentially susceptible to the nematode and bacterium.  Livestock deaths and production losses to annual ryegrass toxicity (ARGT) disease are caused by corynetoxins produced by R. toxicus and vectored by A. funesta.  Most valuable susceptible livestock include cattle, sheep and horses. Domestic and international trade are likely to be negatively impacted.

Worldwide Distribution:  North America: USA (Oregon); Oceania: Australia;

Official Control: Presently, Anguina funesta is on the ‘Harmful Organism List’ for Lolium spp. and L. temulentus seeds intended for export to Chile, while Anguina spp. is on the ‘Harmful Organism List’ for Australia, Namibia, Nauru, and South Africa (USDA-PCIT, 2017).  The USDA APHIS originally added the Anguina spp.-vectored bacterial pathogen, Rathayibacter toxicus to the Select Agent List in 2008, relisted it in 2012 and continues to date.

California Distribution:  Anguina funesta has not been reported from California.

California Interceptions: None reported.

The risk Anguina funesta would pose to California is evaluated below.

Consequences of Introduction: 

1) Climate/Host Interaction: If allowed introduction, Anguina funesta is likely to establish a widespread distribution wherever annual ryegrass and fescue grass are able to grow throughout California. The grasses are commonly grown in commercial, private, and agricultural environments within the State.

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: The host range is limited to annual ryegrass (Lolium rigidum) and fescue grasses (Festuca spp. and Vulpia).  Only L. rigidum and V. myuros are natural hosts of the nematode pathogen.

Evaluate the host range of the pest.

Score: 1

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: The nematode is spread over short and long distances mainly through artificial means. The primary means of spread is through galls intermixed with non-cleaned or poorly cleaned grass seed lots.  They can also be spread by wind and in hay.  Other means of spread include infested soil/gall contaminated machinery, vehicles, humans and animals or run-off water.   The nematodes have high reproductive potential and are capable of surviving in dry state within seeds for many years, thus enhancing spread over long durations.

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 funesta infestations resulting in seed galls, could potentially lower crop yield, increase costs of crop production, trigger loss of markets including establishment of quarantines, and change normal cultural practices.  Furthermore, the nematode species is a vector of bacterial pathogen, Rathayibacter toxicus that causes Rathayibacter poisoning or annual ryegrass toxicity (ARGT) disease resulting in death of agricultural livestock.  Therefore, a high rating is given to this category.

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

Economic Impact: A, B, C, D, E, F.

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 funesta may significantly affect residential and commercial turf gardens.  Annual ryegrass may also be used in agricultural and other environments as a cover crop to prevent soil erosion, improve soil structure and drainage, suppress weeds, and improve organic content of soil. Infestation of the nematode species could impact these environments and consequently trigger additional official or private treatment programs.  A ‘High’ rating is given to 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.

Environmental Impact Score: 3

– 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.

Consequences of Introduction to California for Anguina funesta:  High (13)

Add up the total score and include it here.

 -Low = 5-8 points

 -Medium = 9-12 points

 –High = 13-15 points

Total points obtained on evaluation of consequences of introduction of Anguina funesta to California = 13.

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.

Evaluation is ‘Not established in California’.  

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:

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

Final Score:  Score of Consequences of Introduction – Score of Post Entry Distribution and Survey Information = 13



Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for the seed gall nematode, Anguina funesta is A.


Alderman S. C. et al. 2003.  Use of a seed scarifier for detection and enumeration of galls of Anguina and Rathayibacter species in Orchard grass seed.  Plant Disease 87:320-323.

Kessell, D.  2010.  Annual ryegrass toxicity – current situation.  Department of Agriculture and Food, Government of Western Australia, Note: 417.

Murray, T. D., I. Agarkova, S. Alderman, J. Allen, R. Bulluck, J. Chitambar, C. Divan, I. Riley, B. Schroeder, A. Sechler, and S. Subbotin. 2014. Recovery Plan for Rathayibacter Poisoning caused by Rathayibacter toxicus (syn. Clavibacter toxicus) National Plant Disease Recovery System, a cooperative project of The American Phytopathological Society and The United States Department of Agriculture, posted at  Updated March 2015.

ODA.  2011.  2011 Plant Health Section Annual Report Commodity Inspection Division. State of Oregon Department of Agriculture.

Price, P. C., Fisher, J. M. and Kerr, A.  1979.  On Anguina funesta n. sp. and its association with Corynebacterium sp., in infecting Lolium rigidium.  Nematologica 25:76-85.

Putnam M. L.  2011.  Rathyibacter toxicus, select agent.  Oregon State University Plant Clinic, Corvallis, Oregon (Poster).

Riley, I. T. and Barbetti, M. J.  2008.  Australian anguinids: their agricultural impact and control.  Australasian Plant Pathology 37:289-297.

Riley, I. T. and McKay, A. C.  1990.  Specificity of the adhesion of some plant pathogenic microorganisms to the cuticle of nematodes in the genus Anguina (Nematoda: Anguinidae).  Nematologica 36:90-103.

SON.  (Not dated).  Anguina funesta Pest Information.  Exotic Nematode Plant Pests of Agricultural and Environmental significance to the United States.  The Society of Nematologists.

Subbotin, S. A. et al.  2003.  Evolution of the gall-forming plant parasitic nematodes (Tylenchida: Anguinidae) and their relationships with hosts as inferred from Internal Transcribed Spacer sequences of nuclear ribosomal DNA.  Molecular Phylogenetics and Evolution 30:226-235.

Subbotin, S. A. and I. T. Riley.  Stem and gall forming nematodes. In Practical Plant Nematology.  Eds. Manzanilla-Lopez R., and M. Marban-Mendoza.  Biblioteca Básica de Agricultura, Grupo Mundi-Prensa, Mexico.  521-577 pp.

USDA PCIT.  2017.  USDA Phytosanitary Certificate Issuance & Tracking System. May 24, 2017, 11:51:23 am CDT.

Responsible Party:

John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-262-1110,

Comment Period: CLOSED

6/5/2017 – 7/20/2017

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Pest Rating: A 

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