Ditylenchus dipsaci (Kühn, 1857) Filipjev, 1936

California Pest Rating for

Ditylenchus dipsaci (Kühn, 1857) Filipjev, 1936

Pest Rating: C

PEST RATING PROFILE

Initiating Event:

None. The current rating and status of Ditylenchus dipsaci in California are re-evaluated.

History & Status:

Background: During the 1920s, the stem and bulb nematode was one of the earliest nematodes known to affect garlic and narcissus production in California where it continues to be a major pest of garlic, onion and alfalfa (Siddiqui, 1973). In alfalfa, damage is most severe in moist, cool weather in cooler, sprinkler-irrigated inland valley and foggy coastal areas of California, and the nematode may be found as far south in the Central Valley as Madera County (Westerdahl, 2007). Ditylenchus dipsaci, the stem and bulb nematode, is one of the most devastating plant parasitic nematodes on a wide range of plants and is distributed worldwide especially in temperate regions. It is a migratory endoparasitic nematode that feeds and inhabits mostly aerial parts of host plants (stems, leaves, inflorescence, seeds) but also invades below ground modified parts (bulbs, tubers, stolons, rhizomes and rarely roots). Ditylenchus dipsaci has been documented in early reports as a complex containing several species (Sturhan and Brzeski, 1991). However, D. dipsaci sensu stricto can now be distinguished from other related species by host plant range, chromosome number, morphometric values and gene sequences (Subbotin et al., 2005).

Disease cycle: D. dipsaci completes a life cycle from egg to egg in about 21 days at 59°F and a female lays 200-500 eggs within garlic and onion tissue, and egg development occurs between 59 and 70°F (Becker and Westerdahl, 2018). Several generations can occur over one growing season. Under favorable moisture and temperature conditions, preadults become active, swim in films of water in soil or on wet plant surfaces, and attack a germinating seed or seedling entering near the root cap or within the seed. Nematodes remain intercellular and feed on parenchymatous tissue causing cell division and enlargement. In young plants, the nematodes enter leaves through stomata or directly through the epidermis in leaf bases – resulting in cell enlargement, disappearance of chloroplasts, and increase in intercellular spaces. As bulbs enlarge, the nematodes move down the leaves intercellularly or on the surface of leaves and re-entering at the outer sheaths of the stem or neck to infect the outer scales of bulbs. Middle lamellae of cells and cells break down forming large cavities and stems lose their rigidity and collapse. Nematodes continue to feed through the parenchymatous outer scales. The macerated tissue has a white mealy texture but soon turn brown due to secondary invasion. In early stages the nematodes remain within individual scales causing complete or incomplete rings of frosty white or brown tissue. Later, the nematodes infect more scales even after harvest and in storage usually resulting in totally infecting a bulb. When heavily infected bulbs decay, preadults exit and accumulate about the basal plates of dried bulbs as cottony masses called “nematodes wool” and can survive there for years (Agrios, 2005; Westerdahl and Becker, 2018). Survival: The pre-adults or fourth stage larvae can survive freezing or extreme dry conditions in anhydrous state for long periods in plant tissue, stems, leaves, bulbs, seeds or in soil (Agrios, 2005).

Dispersal and spread: Infested plant material including bulbs, stems, leaves, and seeds; infested soil, contaminated cultivation tools and equipment, contaminated irrigation and splash water.

Hosts: There are more than 500 plant species in over 40 angiosperm families that are known to be hosts of D. dipsaci. Many of the biological races of D. dipsaci have limited host ranges (EPPO, 2008). In California, D. dipsaci is an important nematode pest particularly of onion, garlic, and alfalfa.

Symptoms: Emergence of infected onion seedlings is retarded, with reduced stands, appearing pale green to yellow, twisted and arched and collapsed. Most infected seedlings die within three or more weeks. Developing plants exhibit stunting, light yellow or brown spots, swellings (spikkles) and open lesions, swollen and deformed stems, thickened, curled, distorted leaves, collapse of leaves and premature drying and defoliation; and bloated tissue with a spongy appearance, leaf tips often exhibit a gray to brown dieback. Older plants may also die before harvest.

Bulb tissue begins softening at the neck and gradually proceeds downwards. Young bulbs are soft, swollen and malformed, and exhibit a coarse-textured tissue beneath the outer scale. Bulb scales appear pale gray, soft, and loose. Bulb tissue underneath the loose outer scales is soft, puffy, mealy and frosty in appearance. Affected scales appear as discolored rings in cross sections of infected bulbs, and as irregular, discolored lines in longitudinal sections. Individual cloves or, in severe cases, larger areas of the bulb become affected. Bulbs may split, become malformed, or produce sprouts and double bulbs. Under dry conditions bulbs become desiccated, light in weight, odorless, and split at the base. Basal plate and roots of severely infested bulbs may also appear to a have a dry rot and can be easily separated from the bulbs, mimicking symptoms of Fusarium basal plate rot. Under moist conditions, secondary invaders set in and bulbs rots and decay. In storage, bulbs decay (EPPO, 2008).

Carrots and sugar beet: The plant is most affected at 2-4 cm below and above ground level. Early symptoms include straddled (collapsed on both sides) leaves, multi-bud plant crowns and light discoloration of taproot tops (EPPO, 2008).

Alfalfa: Nematodes enter bud tissue and developing buds. Infected stems are enlarged, discolored – later may turn black as nematode numbers increase, swollen nodes, shortened internodes (stunted). Infected plants have fewer shoots, and deformed buds. White or pale flags (destruction of chloroplasts) are formed as nematodes move to leaf tissue (EPPO, 2008).

Seeds: Small seed generally show no symptoms of infestation, but the skin of larger seeds, (Phaseolus vulgaris, Vicia faba), may be shrunken with discolored spots (EPPO, 2008).

Damage Potential: If not controlled, the stem and bulb nematode has the potential to affect host crop production by reducing yield and quality, increasing costs of nematode-free production, and management options. The seedborne capability of D. dipsaci would impact international trade of host seed and planting stock, if the latter were found infested with the nematode. However, California’s Seed Certification Program that ensures the use of clean, nematode-free seeds, has provided California garlic growers a strong preventive measure against the stem and bulb nematode.

Worldwide Distribution: Asia: Armenia, Azerbaijan, China, Republic of Georgia, India, Iran, Iraq, Israel, Japan, Jordan, Kazakhstan, Republic of Korea, Kyrgyzstan, Oman, Pakistan, Syria, Taiwan, Turkey, Uzbekistan, Yemen; Africa: Algeria, Kenya, Morocco, Nigeria, Réunion, South Africa, Tunisia; Europe: Albania, Austria, Belarus, Belgium, Bosnia-Hercegovina, Bulgaria, Croatia, Cyprus, Czech Republic, Czechoslovakia (former), Denmark, Estonia, Finland, France, Germany, Greece, Hungary, Iceland, Ireland, Italy, Latvia, Lithuania, Macedonia, Malta, Moldova, Netherlands, Norway, Poland, Portugal, Romania, Russian Federation, Serbia, Slovakia, Slovenia, Spain, Sweden, Switzerland, United Kingdom, Ukraine, Yugoslavia; North America: Canada, Mexico, USA; Central America and Caribbean: Costa Rica, Dominican Republic, Haiti; South America: Argentina, Bolivia, Brazil, Chile, Colombia, Ecuador, Paraguay, Peru, Uruguay, Venezuela; Oceania: Australia, New Zealand (CABI, 2018).

In the USA it has been reported from several states including: Alabama, Arizona, California, Colorado, Hawaii, Idaho, Michigan, Minnesota, Montana, Nevada, New Hampshire, New York, North Carolina, Ohio, Oregon, South Dakota, Utah, Virginia, Washington, Wyoming (CABI, 2018).

Official Control: Currently, D. dipsaci is on the ‘Harmful Organism Lists’ for 50 countries including: Algeria, Antigua and Barbuda, Bangladesh, Brazil, Canada, Chile, China, Cook Islands, Costa Rica, Cuba, Egypt, El Salvador, European Union, French Polynesia, Georgia, Grenada, Guatemala, Holy See (Vatican City State), Honduras, India, Indonesia, Israel, Jordan, Lebanon, Madagascar, Mexico, Monaco, Morocco, Namibia, New Caledonia, New Zealand, Nicaragua, Norway, Panama, Paraguay, San Marino, Serbia, South Africa, Sri Lanka, Taiwan, United Republic of Tanzania, Thailand, Timor-Leste, Tunisia, Turkey, Uganda, United Arab Emirates, Uruguay, Viet Nam, and Yemen (USDA PCIT, 2018).

California Distribution: Ditylenchus dipsaci is widely distributed in California.

California Interceptions: None.

The risk Ditylenchus dipsaci would pose to California is evaluated below.

Consequences of Introduction:

1) Climate/Host Interaction: Ditylenchus dipsaci is already widespread within California. The state provides suitable hosts and climate for the establishment and spread of dipsaci to uninfected sites.

Evaluate if the pest would have suitable hosts and climate to establish in California. Score: 2

– 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: Ditylenchus dipsaci has a very wide host range comprising more than 500 plant species in over 40 angiosperm families. The species also has several biological races which have limited host ranges. In California, dipsaci is an important nematode pest particularly of onion, garlic, and alfalfa.

Evaluate the host range of the pest. Score: 3

– 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 dispersed artificially mainly through Infested plant material including bulbs, stems, leaves, and seeds; infested soil, contaminated cultivation tools and equipment, contaminated irrigation and splash water. The ability to survive anhydrously over adverse environmental conditions particularly within plant seed and infested planting stock enables dipsaci for long distance movement over extends periods of time.

Evaluate the natural and artificial dispersal potential of the pest.

Score: 2

– 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.

Economic Impact: If left unmanaged, the stem and bulb nematode has the potential to affect host crop production by reducing yield and quality, changing normal cultural practices including supply of irrigation water to field grown crops, and increasing costs of nematode-free production. The seedborne capability of dipsaci would impact international trade of host seed and planting stock, if the latter were found infested with the nematode. However, California’s Seed Certification Program that ensures the use of clean, nematode-free seeds, has provided California garlic growers a strong preventive measure against the stem and bulb nematode, and the use of resistant varieties is regarded the most effective control of D. dipsaci in alfalfa.

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

Economic Impact: A, B, C, D, G

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: Ditylenchus dipsaci has not been reported to have significant environmental impact in California. Home gardening and ornamental plantings are usually protected against the nematode through use of nematode-free planting materials.

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

Environment Impact: None

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. Score:

– 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 Ditylenchus dipsaci:** 11

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 = 11

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 in California.

Score: (-3)

-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 = 8

Uncertainty:

None.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for Ditylenchus dipsaci is C.

References:

Agrios, G. N. 2005. Plant Pathology (Fifth Edition). Elsevier Academic Press, USA. 922 p.

Becker, J. O. and Westerdahl, B. B. 2018. Onion and garlic nematodes. UCIPM Statewide Integrated Pest Management Program, University of California Agriculture and Natural Resources. (Updated 2/07). http://ipm.ucanr.edu/PMG/r584200111.html

CABI. 2018. Ditylenchus dipsaci full datasheet. Crop Protection Compendium. https://www.cabi.org/cpc/datasheet/19287

EPPO. 2008. Ditylenchus destructor and Ditylenchus dipsaci Diagnostics. European and Mediterranean Plant Protection Organization. OEPP/EPPO Bulletin 38: 363-373.

Siddiqui, I. A., Sher, S. A., and French, A. M. 1973. Distribution of plant parasitic nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry, 324 p.

Sturhan, D., and Brzeski, M. W. 1991. Stem and bulb nematodes, Ditylenchus spp. In: Manual of Agricultural Nematology Ed. Nickle, W. R., pp.423–464. Marcel Dekker, Inc., New York (US).

Subbotin, S. A., Madani, M. Krall, E., Sturhan, D., and Moens, M. 2005. Molecular diagnostics, taxonomy, and phylogeny of the stem nematode Ditylenchus dipsaci species complex based on the sequences of the internal transcribed spacer-rDNA. Phytopathology 95: 1308-1315.

USDA PCIT. 2018. USDA Phytosanitary Certificate Issuance & Tracking System. Retrieved July 26, 2018, 1:20:45 pm CDT. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp.

Westerdahl, B. B. 2007. Parasitic nematodes in alfalfa. In Irrigated Alfalfa Management for Mediterranean and Desert Zones. University of California Division of Agriculture and Natural Resources Publication 8297 Chapter 11.

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, plant.health[@]cdfa.ca.gov.

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