Ditylenchus dipsaci (stem and bulb nematode)

Datasheet

Ditylenchus dipsaci (stem and bulb nematode)

Index

Summary

Last modified
10 December 2020

Datasheet Type(s)
Invasive Species
Pest

Preferred Scientific Name
Ditylenchus dipsaci

Preferred Common Name
stem and bulb nematode

Taxonomic Tree
Domain: Eukaryota
Kingdom: Metazoa
Phylum: Nematoda
Class: Secernentea
Order: Tylenchida

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Pictures

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Picture

Title

Caption

Infestation

Stem and bulb nematode (Ditylenchus dipsaci); infestation of nematodes within a narcissus bulb. United Kingdom.

©Central Science Laboratory/Harpenden Archive, British Crown/Bugwood.org - CC BY-NC 3.0 US

Symptoms

Stem and bulb nematode (Ditylenchus dipsaci); damage to stems and bulbs on onion transplants. USA.

©Howard F. Schwartz/Colorado State University/Bugwood.org - CC BY 3.0 US

Symptoms

Stem and bulb nematode (Ditylenchus dipsaci); alfalfa plant showing damage due to infestation. USA.

©Howard F. Schwartz/Colorado State University/Bugwood.org - CC BY 3.0 US

Infested garlic

Garlic bloat nematode (Ditylenchus dipsaci); nematode "wool" found between the bulbs scales of infested garlic. Cornell Plant Disease Diagnostic Clinic, Ithaca, New York, USA.

©Sandra Jensen/Cornell University/Bugwood.org - CC BY-NC 3.0 US

Adult female

Line drawing - Reproduced from Hooper DJ, 1972. CIH Descriptions of Plant-parasitic Nematodes. Set 1, No. 14. Wallingford, UK: CAB International.

©CAB International

Identity

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Preferred Scientific Name

Ditylenchus dipsaci (Kühn, 1857) Filip'ev, 1936

Preferred Common Name

stem and bulb nematode

Other Scientific Names

Anguillula devastatrix Kühn, 1869
Anguillula dipsaci Kühn, 1857
Anguillula secalis Nitschke, 1868
Anguillulina dipsaci (Kühn, 1857) Gervais & Van Beneden, 1859
Anguillulina dipsaci var. communis Steiner & Scott, 1935
Ditylenchus allocotus (Steiner, 1934) Filip'ev & Sch. Stek., 1
Ditylenchus amsinckiae (Steiner & Scott, 1935) Filip'ev & Sch.
Ditylenchus dipsaci var. tobaensis Schneider, 1937
Ditylenchus fragariae Kir'yanova, 1951
Ditylenchus sonchophila Kir'yanova, 1958
Ditylenchus trifolii Skarbilivich, 1958
Tylenchus allii Beijerinck, 1883
Tylenchus devastator
Tylenchus devastatrix (Kühn) Oerley
Tylenchus dipsaci (Kühn, 1857) Bastian, 1865
Tylenchus havensteinii Kühn, 1881
Tylenchus hyacinthi Prillieux, 1881
Tylenchus putrefaciens Kühn, 1879

International Common Names

English: brown ring disease of hyacinth; bulb eelworm; onion bloat; ring disease of bulbs
Spanish: acebollado del centeno; anguilulosis de la avena; anguilulosis de la cebolla; cebollino del centeno; nematodo de la cebolla; nematodo del tallo
French: anguillule commune des tiges; anguillule des cereales et des bulbes; nématode des tiges; poireaute avoine; seigle oignonne

Local Common Names

Denmark: stængelnematod
Finland: varsiankeroinen
Germany: ruebenkopf-älchen; stengel-älchen; stock-älchen
Italy: anguillula delle piante erbacee
Japan: kuki-sentyubyo; nami-kuki-sentyu
Netherlands: stengelaaltje
Norway: stengelnematode
Sweden: stjälknematod
Turkey: sogan sak nematodo

EPPO code

DITYDI (Ditylenchus dipsaci)

Taxonomic Tree

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Domain: Eukaryota
Kingdom: Metazoa
Phylum: Nematoda
Class: Secernentea
Order: Tylenchida
Family: Anguinidae
Genus: Ditylenchus
Species: Ditylenchus dipsaci

Notes on Taxonomy and Nomenclature

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Ditylenchus dipsaci exhibits considerable variation with external factors, such as temperature, and it has several host races. Its chromosome number has been reported from a number of hosts and geographical origins and it varies from n = 6 to 30 (Sturhan and Brzeski, 1991). Not surprisingly, several species have been described with morphological characteristics that fall within the range of variation of D. dispaci. Some of these species are local variants of D. dipsaci and should be treated as synonyms of this species. Others, such as D. phloxidis, are unable to cross with D. dipsaci (Ladygina, 1974) and are considered to be valid species (Fortuner, 1982). Some authors lump all the morphologically indistinguishable species into a collective species, D. dipsaci (Sturhan and Brzeski, 1991). Summarizing several years of studies in Russia on the question (Barabashova, 1972, 1974, 1975, 1976, 1978, 1979; Ladygina, 1974, 1976), Ladygina and Barabashova (1980) consider that two groups may be distinguished in the Ditylenchus dipsaci complex. The parasites of cultivated plants form a fairly homologous group as to morphology and chromosome number (n = 12) in all but the 'giant race', parasitic in Vicia faba var. equina, where n = 27. Most of the races in this first group cross-breed successfully. The second group, parasites of wild plants, forms a heterogeneous group both in karyotype (n = 18 to 28) and morphology. At least partial incompatibility is observed between races in the second group. The two groups are genetically incompatible.

To conclude, there seem to exist two or more valid species in the D. dipsaci complex, but they have not yet been validly or completely described and differentiated.

Description

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Female

Body almost straight when killed by heat. Cuticle marked by transverse annuli about 1 µm apart; lateral fields with 4 lines occupying 1/6-1/8 of body width. Phasmid-like structures are present dorsal to the lateral fields (Sturhan and Rahi, 1996). Lip region low, unstriated, slightly flattened, barely set off from the body. Head framework moderately developed, stylet about 10-12 µm long with distinct basal knobs. Procorpus of oesophagus cylindrical, narrowing slightly as it joins the fusiform median bulb. Isthmus narrow, surrounded by nerve ring where it begins to expand into posterior oesophageal glands that end at, or slightly overlap, the intestine; small valve present at oesophago-intestinal junction. Excretory pore opposite the basal bulb. Tail conoid, 4-5 anal-body widths, with a sharply pointed terminus. Vulva distinct, anterior ovary outstretched with oocytes in a single (rarely double) row, sometimes reaching the oesophageal region. Post-vulval sac present, extending about half-way to the anus.

Male

Anterior region similar to female. Body almost straight when killed by heat. Tail similar to female with sharply pointed terminus; bursa present, beginning opposite the anterior end of the spicules and extending to three quarters of the tail end. Spicules 23-28 µm long, curved ventrally, expanded anteriorly. Gubernaculum short and simple.

Measurements

After Thorne (1945), from teasel (Dipsacus fullonum). Females: L = 1.0-1.3 mm; a = 36-40; b = 6.5-7.1; c = 14-18; V = 80%. Males: L = 1.0-1.3 mm; a = 37-41; b = 6.5-7.3; c = 12-15; T = 65-72.

After Blake in Hooper (1972), from oats (Avena sativa). 48 females: L = 1.3 mm (S.E. = 0.009); a = 62 (S.E. = 5.6); b = 15 (S.E. = 1.4); c = 14 (S.E. = 2.1); V = 80 (S.E. = 1.5). 23 males: : L = 1.3 mm (S.E. = 0.017); a = 63 (S.E. = 11.3); b = 15 (S.E. = 1.7); c = 14 (S.E. = 2.1); T = 72.

After Goodey (1941), giant race from broad bean (Vicia faba). 22 females: L = 1.73-2.23 (1.97) mm; a = 50-64 (58.2); b = 7-12 (9); c = 15.8-20.0 (17.5); V = 76-84 (82). 23 males: L = 1.51-1.93 (1.77) mm; a = 58-74 (67); b = 6-8 (7); c = 14.6-19.1 (16.9).

Distribution

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D. dipsaci occurs locally in most temperate areas of the world (Europe and the Mediterranean region, North and South America, northern and southern Africa, Asia and Oceania) but it does not seem able to establish itself in tropical regions except at higher altitudes that have a temperate climate. In most countries regulatory measures such as certification schemes are applied to minimize further spread of D. dipsaci. There are several reports of presence in India in the literature (Hooper, 1972; Maqbool, 1991; Sturhan and Brzeski, 1991; Chakraborti, 2001; Logani et al., 2002), although others refer to its absence (Sethi et al., 1972; Rajan and Lal, 2004); EPPO (2005) notes that its presence is not confirmed by the national plant protection service. For Saskatchewan, Canada, CABI/EPPO (1999) incorrectly cites Hannah and Hawn (1975) as the source; this is not a report of D. dipsaci in this province. However, D. dipsaci has been reported from the weed Cirsium arvense in Saskatchewan (Watson and Shorthouse, 1979). The authors indicate that a host-specific race may have evolved. See also CABI/EPPO (1998, No. 160).

A record of D. dipsaci in Taiwan (CABI/EPPO, 1999; EPPO, 2006) published in previous editions of the Compendium was incorrect and has been removed. D. dipsaci has not been found in Taiwan by Dr Tsai of National Chung Hsing University, who has conducted several years study of nematode fauna in Taiwan sponsored by The Bureau of Animal and Plant Health Inspection and Quarantine (BAPHIQ).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Last updated: 17 Feb 2021

Continent/Country/Region	Distribution	First Reported	Reference	Notes
Africa
Algeria	Present		Lamberti et al. (1975) Vito et al. (1994a) Troccoli and Vito (2002) Esquibet et al. (2003) CABI and EPPO (2009) EPPO (2020) CABI (Undated)
Kenya	Present, Few occurrences		CABI and EPPO (2009) EPPO (2020)
Morocco	Present, Localized		Schluter (1972) Vito et al. (1994a) Abbad Andaloussi and Bachikh (2001) Troccoli and Vito (2002) Esquibet et al. (2003) CABI and EPPO (2009) Mokrini et al. (2009) EPPO (2020) CABI (Undated)
Nigeria	Absent, Unconfirmed presence record(s)		Ogbuji (1979) EPPO (2020)
Réunion	Present, Few occurrences		Lamberti et al. (1986) CABI and EPPO (2009) EPPO (2020)
South Africa	Present, Localized		Lamprecht et al. (1987) Marais (1990) CABI and EPPO (2009) EPPO (2020)
Tunisia	Present, Few occurrences		Hanounik et al. (1986) Kamel et al. (1989) Vito et al. (1994a) Troccoli and Vito (2002) CABI and EPPO (2009) EPPO (2020)
Asia
Armenia	Present		Pogosyan et al. (1972) Mkrtchyan (1983) CABI and EPPO (2009) EPPO (2020)
Azerbaijan	Present		Kasimova (1969) Kasimova and Atakishieva (1980) CABI and EPPO (2009) EPPO (2020)
China	Present, Localized		Shepherd and Barker (1990) CABI and EPPO (2009) EPPO (2020)
-Gansu	Present		CABI and EPPO (2009) EPPO (2020)
-Hebei	Present		CABI and EPPO (2009) EPPO (2020)
-Henan	Present		CABI and EPPO (2009) EPPO (2020)
-Shandong	Present		CABI and EPPO (2009) EPPO (2020)
-Sichuan	Present		Chen (1993) CABI and EPPO (2009) EPPO (2020)
-Xinjiang	Present		CABI and EPPO (2009) EPPO (2020) CABI (Undated)
Georgia	Present		Matveeva (1972) CABI and EPPO (2009) EPPO (2020)
India	Absent, Unconfirmed presence record(s)		Hooper (1972) Maqbool (1991) Sturhan and Brzeski (1991) EPPO (2020)
-Uttar Pradesh	Absent, Unconfirmed presence record(s)		Ruchi Logani et al. (2002) EPPO (2020)
-West Bengal	Absent, Unconfirmed presence record(s)		Chakraborti (2001)
Iran	Present		Abivardi and Sharafeh (1973) CABI and EPPO (2009) Karani and Karegar (2013) Mahdikhani and Alvani (2013) Esmaeili and Heydari (2016) Azimi (2017) EPPO (2020)
Iraq	Present		Stephan (1989) CABI and EPPO (2009) EPPO (2020)
Israel	Present, Widespread		Nevo (1972) Siti (1980) Aftalion and Cohn (1990) Subbotin et al. (2005) CABI and EPPO (2009) EPPO (2020)
Japan	Present		CABI and EPPO (2009) EPPO (2020)
-Honshu	Present		Saigusa et al. (1972) Kuroki (1987) CABI and EPPO (2009) EPPO (2020)
Jordan	Present		Hashim (1979) Hashim (1979a) Hashim (1983) CABI and EPPO (2009) EPPO (2020)
Kazakhstan	Present		Vladimirova (1975) German and Sagitov (1983) CABI and EPPO (2009) EPPO (2020)
Kyrgyzstan	Present		Matveeva (1972) CABI and EPPO (2009) EPPO (2020)
Oman	Present, Few occurrences	1993	Al-Zidgali et al. (1994) CABI and EPPO (2009) EPPO (2020)
Pakistan	Present		Khan et al. (1987) Khan et al. (2007) CABI and EPPO (2009) EPPO (2020)
South Korea	Present		Choi (1975) Park et al. (1993) Na SeungYong et al. (1998) Park et al. (2005) CABI and EPPO (2009) EPPO (2020) CABI (Undated)
Syria	Present, Few occurrences		Hanounik and Sikora (1980) Greco et al. (1984) Lamberti (1984) Augustin and Sikora (1989) Greco et al. (1992) Akem and Bellar (1999) CABI and EPPO (2009) EPPO (2020)
Taiwan	Absent, Invalid presence record(s)		EPPO (2020) CABI and EPPO (2009) CABI (Undated)
Turkey	Present, Localized		Enneli and Ozturk (1989) Vito et al. (1994) Esquibet et al. (2003) CABI and EPPO (2009) EPPO (2020) CABI (Undated)
Uzbekistan	Present		Karimova (1973) Mavlyanov (1973) Karimova (1986) CABI and EPPO (2009) EPPO (2020)
Yemen	Present, Few occurrences		CABI and EPPO (2009) EPPO (2020)
Europe
Albania	Present		Shepherd and Barker (1990) CABI and EPPO (2009) EPPO (2020)
Austria	Present, Widespread		CABI and EPPO (2009) EPPO (2020)
Belarus	Present		Ivanova (1976) Ivanova (1984) Ilyashenka and Ivaniuk (2008) CABI and EPPO (2009) EPPO (2020)
Belgium	Present		Clamot (1975) Gilles et al. (1979) CABI and EPPO (2009) EPPO (2020)
Bosnia and Herzegovina	Present		Klindic et al. (1978) CABI and EPPO (2009) EPPO (2020)
Bulgaria	Present, Localized		Stoyanov (1975) CABI and EPPO (2009) Samaliev and Mohamedova (2011) EPPO (2020) CABI (Undated)	First reported: 192*
Croatia	Present, Localized		Jelić (1992) CABI and EPPO (2009) EPPO (2020)
Cyprus	Present		Philis (1987) Philis (1995) CABI and EPPO (2009) EPPO (2020)
Czechia	Present, Widespread		Adamova (1975) Kudela (1975) Baier and Balas (1976) Douda (2005) CABI and EPPO (2009) Zouhar et al. (2016) EPPO (2020)
Czechoslovakia	Present		Branzovsky (1973) Vinduska (1976) CABI (Undated)
Denmark	Present, Few occurrences		Hansen et al. (1972) Yeates (1973) Denmark, State Plant Pathology Institute (1976) Knuth (1996) CABI and EPPO (2009) EPPO (2020)
Estonia	Present, Few occurrences		Krall and Krall (1970) Subbotin et al. (2005) CABI and EPPO (2009) EPPO (2020)
Finland	Present, Localized		CABI and EPPO (2009) EPPO (2020)
France	Present, Localized		CABI and EPPO (2009) Caubel (1972) Caubel (1973) Caubel (1973a) Whitehead et al. (1987) Wendt et al. (1994) Esquibet et al. (2003) Subbotin et al. (2005) EPPO (2020) CABI (Undated)
Germany	Present, Widespread		Gentzsch (1973) Homeyer (1973) Kuthe (1974) Whitehead et al. (1987) Subbotin et al. (2005) Mendoza et al. (2008) CABI and EPPO (2009) Mwaura et al. (2015) EPPO (2020)
Greece	Present, Localized		CABI and EPPO (2009) Koliopanos and Vovlas (1977) Vlachopoulos (1994) EPPO (2020) CABI (Undated)
Hungary	Present, Localized		Budai (1977) CABI and EPPO (2009) EPPO (2020)
Iceland	Present, Few occurrences		Siggeirsson and Riel (1975) CABI and EPPO (2009) EPPO (2020)
Ireland	Present, Few occurrences		Anon (1972) CABI and EPPO (2009) EPPO (2020) CABI (Undated)
Italy	Present		CABI and EPPO (2009) Inserra and Lamberti (1972) Tacconi (1972) Greco et al. (1985) Greco et al. (1986) Greco et al. (2002) Esquibet et al. (2003) Subbotin et al. (2005) Vovlas et al. (2011) EPPO (2020) CABI (Undated)
-Sicily	Present		Greco et al. (2002) CABI and EPPO (2009) EPPO (2020)
Latvia	Present		Eglitis and Kaktynya (1970) Eglitis and Kaktynya (1972) CABI and EPPO (2009) EPPO (2020)
Lithuania	Present, Localized		CABI and EPPO (2009) EPPO (2020) CABI (Undated)
Malta	Present, Localized	1976	Lamberti and Dandria (1979) Larizza and Lamberti (1995) CABI and EPPO (2009) EPPO (2020)
Moldova	Present		CABI and EPPO (2009) EPPO (2020)
Netherlands	Present, Localized		NPPO of the Netherlands (2013) Heijbroek (1973) Whitehead et al. (1987) Janssen et al. (1993) Wendt et al. (1994) CABI and EPPO (2009) Jeszke et al. (2015) EPPO (2020)	Present, in all parts of the area where host crops are grown.
North Macedonia	Present		Krnjaic (1978) CABI and EPPO (2009) EPPO (2020)
Norway	Present, Few occurrences		Vestad and Foss (1971) Vestad (1973) CABI and EPPO (2009) EPPO (2020)
Poland	Present, Localized		Brzeski (1972) Radziwinowicz (1972) Kornobis and Wolny (1997) CABI and EPPO (2009) Jeszke et al. (2015) EPPO (2020)
Portugal	Present, Localized		CABI and EPPO (2009) Carmo et al. (1974) Pereira and Santos (1974) EPPO (2020)
-Azores	Present		Sturhan (1973) CABI and EPPO (2009) EPPO (2020)
-Madeira	Absent, Invalid presence record(s)		EPPO (2020)
Romania	Present, Localized		Romascu and Lemeni (1972) CABI and EPPO (2009) EPPO (2020)
Russia	Present		Subbotin et al. (2005) CABI and EPPO (2009) Vovlas et al. (2011) Madani et al. (2015) EPPO (2020)
-Central Russia	Present		CABI and EPPO (2009) EPPO (2020)
-Russian Far East	Present		Glotova (1972) Matveeva (1972) CABI and EPPO (2009) EPPO (2020)
-Siberia	Present		Matveeva (1972) Shpileva (1972)
-Southern Russia	Present		CABI and EPPO (2009) EPPO (2020)
-Western Siberia	Present		CABI and EPPO (2009) EPPO (2020)
Serbia	Present		EPPO (2020) CABI and EPPO (2009)
Serbia and Montenegro	Present		Grujicic (1974) Grujicic (1974a) Grujičić et al. (1985) Ristić et al. (1990) CABI and EPPO (1999)
Slovakia	Present, Widespread		Valocka and Sabova (1974) Valocka and Sabova (1977) Liskova et al. (1988) CABI and EPPO (2009) Háněl (2017) EPPO (2020)
Slovenia	Present, Localized		Douda (2005) CABI and EPPO (2009) EPPO (2020)
Spain	Present, Localized		CABI and EPPO (2009) Talavera and Jiménez (1997) Vovlas et al. (2011) EPPO (2020) CABI (Undated)
-Canary Islands	Absent, Invalid presence record(s)		EPPO (2020)
Sweden	Present, Widespread		Bingefors (1951) Bingefors (1973) Whitehead et al. (1987) CABI and EPPO (2009) EPPO (2020)
Switzerland	Present, Widespread		Nuesch (1971) Graf and Meyer (1973) Vallotton (1976) Whitehead et al. (1987) CABI and EPPO (2009) EPPO (2020)
Ukraine	Present, Localized		Metlitskii (1972) Shcherbak and Skarbilovich (1973) CABI and EPPO (2009) EPPO (2020)
United Kingdom	Present, Widespread		Goodey (1951) Goodey and Hooper (1962) French et al. (1971) Hooper (1971) Whitehead et al. (1987) Griffith et al. (1997) CABI and EPPO (2009) EPPO (2020)
-England	Present, Widespread		EPPO (2020) Goodey (1951) Brown (1958) Lester and Large (1958) Wallace (1962) Oliff et al. (1969) Hooper (1971) Southey (1971) Whitehead and Tite (1972) Lewis (1979) Whitehead et al. (1979) Whitehead et al. (1983) Cook et al. (1992) Wendt et al. (1994)
-Scotland	Present, Widespread		Goodey (1951) CABI and EPPO (2009) EPPO (2020) Boag (Undated)
-Wales	Present		Cook et al. (1992) Lester and Large (1958)
North America
Canada	Present, Localized		Hawn (1973a) Fushtey and Kelly (1975) Watson and Shorthouse (1979) CABI and EPPO (2009) Madani et al. (2015) Hajihassani et al. (2016) Hajihassani et al. (2017) EPPO (2020)
-Alberta	Present		Hawn (1973) Hawn (1973a) CABI and EPPO (2009) EPPO (2020)
-British Columbia	Present		CABI and EPPO (2009) EPPO (2020) CABI (Undated)
-Manitoba	Present		Hajihassani et al. (2016)
-Ontario	Present		Johnson and Kayler (1972) Fushtey and Kelly (1975) CABI and EPPO (2009) Madani et al. (2015) Hajihassani et al. (2016) Hajihassani et al. (2017) EPPO (2020)
-Prince Edward Island	Present		CABI and EPPO (2009) EPPO (2020)
-Quebec	Present		CABI and EPPO (2009) Madani et al. (2015) EPPO (2020)
-Saskatchewan	Present, Few occurrences		Watson and Shorthouse (1979) CABI and EPPO (2009) EPPO (2020)
Costa Rica	Present		CABI and EPPO (2009) EPPO (2020)
Dominican Republic	Present, Localized		Kermarrec and Belliard (1977) CABI and EPPO (2009) EPPO (2020)
Haiti	Present, Localized		CABI and EPPO (2009) EPPO (2020)
Mexico	Present, Widespread		Pacheco Covarrubias (1986) CABI and EPPO (2009) EPPO (2020) CABI (Undated)
United States	Present, Widespread		Steiner (1938) Krusberg (1961) Edwards and Taylor (1963) Hussey and Krusberg (1970) Evans et al. (1971) Chitwood and Krusberg (1977) Schnabelrauch et al. (1980) Boelter et al. (1985) Griffin (1990) Griffin (1991) Westerdahl et al. (1991) Wendt et al. (1994) Simmons et al. (2008) CABI and EPPO (2009) Mollov et al. (2012) Testen et al. (2014) Madani et al. (2015) French et al. (2017) EPPO (2020)
-Alabama	Present		Gray et al. (1980) CABI and EPPO (2009) EPPO (2020)
-Arizona	Present		Gray et al. (1976) Gray et al. (1994) CABI and EPPO (2009) EPPO (2020)
-California	Present		Viglierchio et al. (1973) Hart (1976) Westerdahl et al. (1991) CABI and EPPO (2009) EPPO (2020)
-Colorado	Present		Gray et al. (1994) Simmons et al. (2008) CABI and EPPO (2009) EPPO (2020)
-District of Columbia	Present		Steiner (1938)
-Florida	Absent, Invalid presence record(s)		EPPO (2020) CABI and EPPO (2009)
-Hawaii	Present		BERGQUIST and RIEDEL (1972) CABI and EPPO (2009) EPPO (2020) CABI (Undated)
-Idaho	Present		Gray et al. (1994) CABI and EPPO (2009) EPPO (2020)
-Illinois	Present		Edwards and Taylor (1963)
-Michigan	Present		Hanna (1971) Schnabelrauch et al. (1980) CABI and EPPO (2009) EPPO (2020)
-Minnesota	Present		EPPO (2020) Mollov et al. (2012) Madani et al. (2015)
-Montana	Present		Gray et al. (1994) CABI and EPPO (2009) EPPO (2020)
-Nevada	Present		CABI and EPPO (2009) EPPO (2020)
-New Hampshire	Present		CABI and EPPO (2009) EPPO (2020)
-New Mexico	Present, Few occurrences		EPPO (2020) French et al. (2017)
-New York	Present		Chitwood and Krusberg (1977) CABI and EPPO (2009) EPPO (2020)
-North Carolina	Present		Steiner (1938) Krusberg (1961) Hussey and Krusberg (1970) Muse and Muse (1972) Chitwood and Krusberg (1977) CABI and EPPO (2009) EPPO (2020)
-Ohio	Present		Testen et al. (2014) EPPO (2020)
-Oregon	Present		Gray et al. (1994) CABI and EPPO (2009) EPPO (2020)
-South Dakota	Present		Gray et al. (1994) CABI and EPPO (2009) EPPO (2020)
-Utah	Present		Campbell and Griffin (1973) Campbell and Griffin (1975) Griffin (1990) Griffin (1991) Gray et al. (1994) CABI and EPPO (2009) EPPO (2020)
-Virginia	Present		CABI and EPPO (2009) EPPO (2020) CABI (Undated)
-Washington	Present		Evans et al. (1971) Gray et al. (1994) Wendt et al. (1994) CABI and EPPO (2009) EPPO (2020)
-Wyoming	Present		Gray et al. (1984) Boelter et al. (1985) Franc et al. (1993) CABI and EPPO (2009) EPPO (2020)
Oceania
Australia	Present, Localized		Stanton et al. (1984) Taylor and Szot (2000) Esquibet et al. (2003) CABI and EPPO (2009) EPPO (2020)
-New South Wales	Present		France, European and Mediterranean Plant Protection Organization (1977) CABI and EPPO (2009) EPPO (2020)
-Queensland	Present		CABI and EPPO (2009) EPPO (2020)
-South Australia	Present		Stirling (1972) Dube (1975) Stanton et al. (1984) Taylor and Szot (2000) CABI and EPPO (2009) EPPO (2020)
-Tasmania	Present		CABI and EPPO (2009) EPPO (2020)
-Victoria	Present		CABI and EPPO (2009) EPPO (2020)
-Western Australia	Present		CABI and EPPO (2009) EPPO (2020)
New Zealand	Present, Widespread		Knight et al. (2002) CABI and EPPO (2009) EPPO (2020) CABI (Undated)
South America
Argentina	Present	1929	Mareggiani and Russo (1992) Doucet (1999) CABI and EPPO (2009) EPPO (2020) CABI (Undated)
Bolivia	Present		CABI and EPPO (2009) EPPO (2020) CABI (Undated)
Brazil	Present		Becker (1999) Subbotin et al. (2005) CABI and EPPO (2009) EPPO (2020)
-Minas Gerais	Present		Charchar et al. (1980) Silva and Campos (1991) CABI and EPPO (2009) EPPO (2020)
-Paraiba	Present		Lopes and Lordello (1980) CABI and EPPO (2009) EPPO (2020)
-Parana	Present		Silva and Santos (1984) Silva and Carneiro (1992) CABI and EPPO (2009) EPPO (2020)
-Rio Grande do Sul	Present		CABI and EPPO (2009) EPPO (2020) CABI (Undated)
-Santa Catarina	Present		Charchar et al. (1980) Becker (1993) Becker (1999) CABI and EPPO (2009) EPPO (2020)
-Sao Paulo	Present		Curi et al. (1984) CABI and EPPO (2009) EPPO (2020)
Chile	Present, Widespread		Bruna V. and Guinez S. (1980) Lamberti et al. (1988) CABI and EPPO (2009) EPPO (2020)
Colombia	Present		Perdomo P. et al. (1984) CABI and EPPO (2009) EPPO (2020)
Ecuador	Present, Localized		Bridge (1975) Bridge (1976) CABI and EPPO (2009) EPPO (2020)
Paraguay	Present, Localized		Shepherd and Barker (1990) CABI and EPPO (2009) EPPO (2020)
Peru	Present		CABI and EPPO (2009) EPPO (2020) CABI (Undated)
Uruguay	Present, Widespread		Minagawa and Maeso-Tozzi (1990) CABI and EPPO (2009) EPPO (2020)
Venezuela	Present		Meredith (1977) CABI and EPPO (2009) EPPO (2020)

Risk of Introduction

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RISK CRITERIA CATEGORY

ECONOMIC IMPORTANCE High
DISTRIBUTION Worldwide
SEEDBORNE INCIDENCE Low
SEED TRANSMITTED Yes
SEED TREATMENT Yes

OVERALL RISK High

Notes on phytosanitary risk

At present, the distribution of the different races throughout the region is patchy and some countries apply official control measures to limit spread. Other countries regard the pest as being a quality pest which can be effectively controlled by production and use of healthy planting material. Without control, D. dipsaci may cause complete failure of host crops within the EPPO region. EPPO lists it as an A2 quarantine pest. CPPC, IAPSC and NAPPO also consider it to be of quarantine significance.

The implementation of certification schemes for the production of host plants of D. dipsaci can provide planting material free from the pest. Imports of soil and plants for planting and seeds of host plants from countries where this nematode occurs should be restricted. See Anselme (1975) for international phytosanitary regulations for seeds.

Hosts/Species Affected

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D. dipsaci is known to attack over 450 different plant species, including many weeds (Goodey et al., 1965). However, it occurs in more than 20 biological races, some of which have a limited host range. The races that breed on rye, oats and onions seem to be polyphagous and can also infest several other crops, whereas those breeding on lucerne, Trifolium pratense and strawberries are virtually specific for their named hosts and appear to have relatively few alternative host plants. The tulip race will also infest Narcissus, whereas another race commonly found in Narcissus does not breed on tulip. It is known that some of the races can interbreed and that their progeny have different host preferences. See also Sturhan (1969) and Eriksson (1974). Sturhan and Brzeski (1991) briefly described 23 races, and three races that were raised to species or subspecies rank (Ditylenchus dipsaci falcariae, D. galeopsidis and D. sonchophila).

In addition to the hosts listed, Gnaphalium spicatum, Oxalis corniculata, Amaranthus deflexus and Eupatorium pauciflorum are reported as wild hosts of D. dipsaci.

Host Plants and Other Plants Affected

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Plant name	Family	Context	References
Aethusa cynapium	Cardiidae	Unknown	Brown (1958)
Allium	Liliaceae	Main
Allium cepa (onion)	Liliaceae	Main	Aftalion and Cohn (1990); Abbad and Bachikh (2001); Bingefors (1951); Bridge (1976); Chitwood and Krusberg (1977); Doncaster (1976); Esquibet et al. (2003); Fushtey and Kelly (1975); Jeszke et al. (2015); Lamberti et al. (1988); Larizza and Lamberti (1995); Subbotin et al. (2005); Whitehead and Tite (1972)
Allium cepa var. aggregatum (shallot)	Liliaceae	Other
Allium porrum (leek)	Liliaceae	Main
Allium sativum (garlic)	Liliaceae	Main	Aftalion and Cohn (1990); Abbad and Bachikh (2001); Douda (2005); Fushtey and Kelly (1975); Madani et al. (2015); Mollov et al. (2012); Subbotin et al. (2005); Testen et al. (2014); Yuksel (1960)
Amberboa moschata	Psittacidae	Unknown	Brown (1958)
Ammi majus (Bishop's-weed)	Apiaceae	Unknown	Greco et al. (2002)
Apium graveolens (celery)	Apiaceae	Other
Asphodelus ramosus		Unknown	Hashim (1979)
Astrantia	Apiaceae	Wild host
Avena fatua (wild oat)	Poaceae	Unknown	Greco et al. (2002)
Avena sativa (oats)	Poaceae	Main	Abbad and Bachikh (2001); Bingefors (1951); Pereira and Santos (1974); Esquibet et al. (2003); Stanton et al. (1984); Subbotin et al. (2005); Wallace (1962)
Avena sterilis (winter wild oat)	Poaceae	Wild host	Abbad and Bachikh (2001)
Avena strigosa (black oat)	Poaceae	Unknown	Aftalion and Cohn (1990)
Begonia	Begoniaceae	Main
Bergenia (elephant-leaved saxifrage)	Saxifragaceae	Wild host
Beta vulgaris (beetroot)	Chenopodiaceae	Unknown	Abbad and Bachikh (2001); Esquibet et al. (2003); Mendoza et al. (2008); Mwaura et al. (2015); Subbotin et al. (2005)
Beta vulgaris var. saccharifera (sugarbeet)	Chenopodiaceae	Main
Brassica napus var. napus (rape)	Brassicaceae	Other
Brassica nigra (black mustard)	Brassicaceae	Unknown	Edwards and Taylor (1963); Greco et al. (2002)
Brassica rapa subsp. rapa (turnip)	Brassicaceae	Wild host
Calceolaria polyrhiza		Unknown	Southey (1971)
Callistephus chinensis (China aster)	Asteraceae	Unknown	Brown (1958)
Cannabis sativa (hemp)	Cannabaceae	Main
Carduus acanthoides (Welted thistle)	Asteraceae	Other
Chenopodium murale (nettleleaf goosefoot)	Chenopodiaceae	Wild host
Cicer arietinum (chickpea)	Fabaceae	Unknown	Abbad and Bachikh (2001)
Cichorium endivia (endives)	Asteraceae	Unknown	Jeszke et al. (2015)
Cichorium intybus (chicory)	Asteraceae	Unknown	Douda (2005)
Cirsium arvense (creeping thistle)	Asteraceae	Wild host	Watson and Shorthouse (1979)
Convolvulus arvensis (bindweed)	Convolvulaceae	Wild host
Crocus sativus (saffron)	Iridaceae	Other
Cucurbita pepo (marrow)	Cucurbitaceae	Unknown	Philis (1995); Wendt et al. (1994)
Cucurbitaceae (cucurbits)	Cucurbitaceae	Other
Daucus carota (carrot)	Apiaceae	Unknown	Abbad and Bachikh (2001); Esquibet et al. (2003)
Dianthus caryophyllus (carnation)	Caryophyllaceae	Other
Digitalis lutea	Scrophulariaceae	Unknown	Subbotin et al. (2005)
Diplotaxis erucoides	Brassicaceae	Unknown	Greco et al. (2002)
Dipsacus		Unknown	Goodey (1951)
Dipsacus fullonum (common teasel)	Dipsacaceae	Unknown	Wendt et al. (1994)
Fragaria (strawberry)	Rosaceae	Unknown	Goodey (1951); Subbotin et al. (2005)
Fragaria ananassa (strawberry)	Rosaceae	Main	Lewis (1979); Madani et al. (2015); Goodey (1951); Park et al. (2005); Samaliev and Mohamedova (2011)
Galium aparine (cleavers)	Rubiaceae	Unknown	Greco et al. (2002)
Gladiolus hybrids (sword lily)	Iridaceae	Main
Helianthus annuus (sunflower)	Asteraceae	Other	Koliopanos and Vovlas (1977)
Heuchera	Saxifragaceae	Unknown	Jeszke et al. (2015)
Hibiscus trionum (Venice mallow)	Malvaceae	Unknown	Edwards and Taylor (1963)
Hordeum vulgare (barley)	Poaceae	Unknown	Philis (1995)
Hyacinthus orientalis (hyacinth)	Liliaceae	Main
Hydrangea (hydrangeas)	Hydrangeaceae	Other
Ipomoea batatas (sweet potato)	Convolvulaceae	Other
Iris latifolia		Unknown	Hastings and Bosher (1938)
Iris tingitana		Unknown	Hastings and Bosher (1938)
Lamium album (white deadnettle)	Lamiaceae	Wild host
Lamium amplexicaule (henbit deadnettle)	Lamiaceae	Wild host
Lamium maculatum (Spotted deadnettle)	Lamiaceae	Unknown	Southey (1971)
Lamium purpureum (purple deadnettel)	Lamiaceae	Wild host
Lens culinaris		Unknown	Abbad and Bachikh (2001); Vito et al. (1994); Greco et al. (1992)
Lens culinaris subsp. culinaris (lentil)	Fabaceae	Other
Lolium perenne (perennial ryegrass)	Poaceae	Unknown	Greco et al. (2002)
Lycoris radiata		Unknown	Steiner (1938)
Lysimachia punctata	Primulaceae	Unknown	Southey (1971)
Lysimachia vulgaris	Primulaceae	Unknown	Subbotin et al. (2005)
Medicago sativa (lucerne)	Fabaceae	Main	Abivardi and Sharafeh (1973); Abbad and Bachikh (2001); Boelter et al. (1985); Chitwood and Krusberg (1977); Evans et al. (1971); Lamberti et al. (1988); Lamprecht et al. (1987); Philis (1995); Simmons et al. (2008); Subbotin et al. (2005); Wendt et al. (1994); Wood and Close (1974)
Monarda		Unknown	Southey (1971)
Myriophyllum verticillatum (whorled watermilfoil)	Haloragidaceae	Wild host
Narcissus (daffodil)	Liliaceae	Main	Hesling (1967); Thomas (1958); Westerdahl et al. (1991); Windrich (1970)
Narcissus pseudonarcissus (wild lent lily)	Liliaceae	Main
Nerine sarniensis (guernsey lily)	Liliaceae	Wild host
Nicotiana tabacum (tobacco)	Solanaceae	Main
Onobrychis viciifolia (sainfoin)	Fabaceae	Other
Orobanche crenata (crenate broomrape)	Orobanchaceae	Unknown	Abbad and Bachikh (2001)
Papaver argemone	Papaveraceae	Unknown	Abbad and Bachikh (2001)
Penstemon	Scrophulariaceae	Unknown	Southey (1971)
Persicaria pensylvanica	Polygonaceae	Unknown	Edwards and Taylor (1963)
Petroselinum crispum (parsley)	Apiaceae	Other
Phalaris canariensis (Canarygrass)	Poaceae	Unknown	Aftalion and Cohn (1990)
Phaseolus (beans)	Fabaceae	Main
Phaseolus coccineus (runner bean)	Fabaceae	Other
Phaseolus vulgaris (common bean)	Fabaceae	Unknown	Philis (1995)
Phlox	Polemoniaceae	Unknown	Madani et al. (2015)
Phlox drummondii (Annual phlox)	Polemoniaceae	Main	Subbotin et al. (2005)
Phlox paniculata (summer perennial phlox)	Polemoniaceae	Main	Jeszke et al. (2015)
Pilosella officinarum (mouse-ear hawkweed)	Asteraceae	Wild host
Pimpinella anisum (aniseed)	Apiaceae	Other
Pisum sativum (pea)	Fabaceae	Main	Abbad and Bachikh (2001); Vito et al. (1994)
Plantago lanceolata (ribwort plantain)	Plantaginaceae	Unknown	Knight et al. (2002); Subbotin et al. (2005)
Polygonum persicaria (redshank)	Polygonaceae	Unknown	Edwards and Taylor (1963)
Polyphagous (polyphagous)		Main
Ranunculus arvensis (Corn buttercup)	Ranunculaceae	Wild host
Raphanus raphanistrum (wild radish)	Brassicaceae	Wild host
Rumex crispus (curled dock)	Polygonaceae	Unknown	Edwards and Taylor (1963)
Saponaria officinalis (soapwort)	Caryophyllaceae	Unknown	Edwards and Taylor (1963)
Secale cereale (rye)	Poaceae	Main	Bingefors (1951); Esquibet et al. (2003)
Silene latifolia subsp. alba (white campion)	Caryophyllaceae	Unknown	Brown (1958)
Sinapis arvensis (wild mustard)	Brassicaceae	Unknown	Abbad and Bachikh (2001)
Solanum americanum	Solanaceae	Unknown	Edwards and Taylor (1963)
Solanum carolinense (horsenettle)	Solanaceae	Unknown	Edwards and Taylor (1963)
Solanum tuberosum (potato)	Solanaceae	Main	Ilyashenka and Ivaniuk (2008); Southey (1971); Wendt et al. (1994)
Sonchus arvensis (perennial sowthistle)	Asteraceae	Unknown	Brown (1958)
Spinacia oleracea (spinach)	Chenopodiaceae	Other
Stellaria media (common chickweed)	Caryophyllaceae	Wild host
Tanacetum coccineum (common pyrethrum)	Asteraceae	Unknown	Brown (1958)
Taraxacum officinale complex (dandelion)	Asteraceae	Wild host
Trifolium pratense (red clover)	Fabaceae	Main	Cook et al. (1992); Grandison (1965); Lester and Large (1958); Mercer and Campbell (1986); Subbotin et al. (2005); Wendt et al. (1994)
Trifolium repens (white clover)	Fabaceae	Main	Cook et al. (1992); Cooper (1989); Cooper and Williams (1983); Grandison (1965); Hay (1995); Hay and Regnault (1995); Mercer and Campbell (1986); Widdup and Williams (1982); Williams and Cooper (1980)
Triticum (wheat)	Poaceae	Other	Lamberti (1984)
Triticum aestivum (wheat)	Poaceae	Unknown	Abbad and Bachikh (2001)
Tulipa (tulip)	Liliaceae	Main
Tulipa gesneriana	Liliaceae	Unknown	Hesling (1972); Wendt et al. (1994)
Veronica gentianoides	Scrophulariaceae	Unknown	Subbotin et al. (2005)
Vicia faba (faba bean)	Fabaceae	Main	Abbad and Bachikh (2001); Pereira and Santos (1974); Vito et al. (1994); Doncaster (1976); Esquibet et al. (2003); Lamberti (1984); Philis (1995); Subbotin et al. (2005); Wendt et al. (1994)
Vicia sativa (common vetch)	Fabaceae	Unknown	Philis (1995)
Zea mays (maize)	Poaceae	Main	Abbad and Bachikh (2001); Subbotin et al. (2005)

Growth Stages

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Flowering stage, Post-harvest, Pre-emergence, Seedling stage, Vegetative growing stage

Symptoms

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In general, this nematode causes swellings and distortion of aerial plant parts and necrosis or rotting of stem bases, bulbs, tubers and rhizomes (see section on Biology).

Allium spp. (onions, garlic, leeks, etc.)

Penetration of onion leaves by D. dipsaci causes leaf deformation and leaf swellings or blister-like areas on the surface. The leaves grow in a disorderly fashion, often hang as if wilted and become chlorotic. Young plants can be killed by high infestations. The inner scales of the bulb are usually more severely attacked than the outer scales. As the season advances the bulbs become soft and when cut open show browning of the scales in concentric circles. Conversely, D. dipsaci on garlic does not induce deformation or swellings, but causes leaf yellowing and death (Netscher and Sikora, 1990).

Lucerne

The crop declines in patches in the field and damage is more serious in humid climates. The whole plant becomes desiccated and presents symptoms of stunting and swelling at the base of the stem with conspicuous shortened internodes. With heavy infestation, plants can be killed.

Tobacco

Invasion by the nematode of the lower part of the stem causes stunting and deformation of the plant followed by 'stem break'.

Faba beans, Vetch, Chickpea, Pea and Lentil

D. dipsaci causes swelling and deformation of stem tissue or lesions which turn reddish-brown then black, depending on cultivar and environmental factors. Newly formed pods take on a dark-brown appearance. The lesions envelop the stem and increase in length, often advancing to the edge of an internode. Leaf and petiole necrosis is also common under heavy infestations, but can be confused with symptoms induced by fungal leaf pathogens. Infected seeds are darker, distorted, smaller in size and may have speckle-like spots on the surface. Heavy infestations often kill the main shoots, stimulating secondary tiller formation. The more severe symptoms are usually induced by the 'giant race' on faba beans (Sikora and Greco, 1990). On faba bean (V. faba), D. dipsaci induces necrosis or swelling of the tissue. Infested stems of lentil and vetch (Vicia spp.) are swollen and show shortened internodes. D. dispaci induces local necrosis on pea and a total necrosis of the stem on vetch (Caubel et al., 1998).

Cereals (oats and rye)

D. dispaci causes the production of extra tillers at the base and the plants become swollen to give a typical 'tulip-root' appearance.

Narcissus

Narcissus leaves are distorted and often have characteristic pale swellings called 'spikkels'; infested bulbs usually have brown rings when sliced.

List of Symptoms/Signs

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Sign	Life Stages	Type
Leaves / abnormal colours
Leaves / abnormal forms
Leaves / abnormal patterns
Leaves / necrotic areas
Seeds / discolorations
Seeds / lesions on seeds
Stems / discoloration of bark
Stems / stunting or rosetting
Vegetative organs / internal rotting or discoloration
Whole plant / dwarfing
Whole plant / plant dead; dieback

Biology and Ecology

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D. dipsaci is a migratory endoparasite that feeds upon parenchymatous tissue in stems and bulbs, causing the breakdown of the middle lamellae of cell walls. Feeding often causes swellings and distortion of aerial plant parts (stems, leaves, flowers) and necrosis or rotting of stem bases, bulbs, tubers and rhizomes. During cold storage of bulbs and tubers, D. dipsaci and rotting may continue to develop.

In onion plants at 15°C, the lifecycle takes approximately 20 days. The duration of the life cycle depends on the temperature and differs among isolates of different origins. Maximum activity and invasive ability is generally between 10 and 20°C. Females lay 200-500 eggs each. Fourth-stage juveniles tend to aggregate on or just below the surface of heavily infested tissue to form clumps of 'eelworm wool' and can survive in dry conditions for several years; they may also become attached to the seeds of host plants such as onions, lucerne, Trifolium pratense, faba beans and Phlox drummondii. In clay soils, D. dipsaci may persist for many years. Cool, moist conditions favour invasion of young plant tissue by this nematode.

For further information on the biology of D. dipsaci, see Seinhorst (1956), Dekker (1969), Hooper and Southey (1978), Sturhan and Brzeski (1991), Griffith et al. (1996, 1997a, b, 1999) and Williams-Woodward and Gray (1999).

Natural enemies

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Natural enemy	Type	Life stages	Specificity	References	Biological control in	Biological control on
Dactylella lysipaga	Predator
Drechmeria coniospora	Pathogen
Hirsutella rhossiliensis	Pathogen
Rhizoglyphus echinopus	Predator

Means of Movement and Dispersal

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In international trade D. dipsaci is liable to be carried on dry seeds and planting material of host plants. In the field the fourth-stage juvenile can withstand desiccation for many years, and although soil densities seem to decrease rapidly, the nematode can survive for years without a host plant. Desiccation of D. dipsaci causes some ultrastructural changes (Wharton, 1996; Wharton and Lemmon, 1998). Following a period of desiccation and re-immersion in water, recovery occurs after a delay (lag phase) showing that repairs or restoration of a normal physiological state are necessary before activity can resume (Wharton et al., 1999). Nematode survival and damage are greater in heavy soils as compared to sandy soils. It can also survive on a number of weeds. Irrigation water and cultivation by contaminated farm tools and machinery are also sources of inoculum dissemination.

Seedborne Aspects

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Incidence

D. dipsaci has been shown to be seedborne on about 15 plant species (Neergaard, 1977). A survey of commercial seeds samples in the UK showed its widespread occurrence in economically important crops including 36-45% of seed stocks of broad been, red beet and carrots, 14-17% of shallots and runner beans and >3% of peas, onions and leeks (Green and Sime, 1979). High incidences of seed infection have been reported, e.g. 67% in broad bean seeds (Steiner and Lamprecht, 1983). Goodey (1945) traced invasion of D. dipsaci through the pedicel and placenta of the onion mother plant into the ovary wall and later through the short funiculus from which the nematodes become attached to the seed primarily in the vicinity of the hilum The nematode has also been located below the seed coat of Vicia faba (Neergaard, 1977). The pathogen was found in 1-40% of V. faba seeds in Algeria (Sellami et al., 1998).

The distribution of D. dipsaci between seeds in infested samples of broad bean seed was shown to be skewed so that the nematodes were concentrated on a few seeds (Green, 1979). Numbers of nematodes within individual seeds may vary substantially. In one of two samples of seed of Vicia faba, all stages of D. dipsaci were found. The other sample (50 seeds) was negative. In 20 seeds of the infected sample there were 20,035 larvae (over 8000 on one seed) (Pereira and Santos, 1975).

Effect on Seed Quality

Infected seeds are darker, distorted, smaller in size and may have speckle-like spots on the surface (Sikora and Greco, 1990).

Pathogen Transmission

Seed

Seed transmission of D. dipsaci to the planted crop is well established. Seinhorst and Koert (1971) found a strong correlation between the number of nematodes/g of seed and percentage of infected onion bulbs. Aerial photography of three fields of lucerne in the UK were used to monitor the spread of a seedborne infestation of D. dipsaci. Results from the use of an image analyser suggested that infestation develops by the generation of additional colonies from the original foci and by the progressive expansion of the area damaged by an established colony (Atkinson and Sykes, 1981). Planting certified nematode-free seeds is recognized as an important control practice for this disease. In Germany, a tolerance level of five nematodes/300 seeds is used to establish the risk of transmission of the pathogen to seedlings (Knuth, 1993).

Other sources

Nematode-infested soil is an important inoculum source of D. dipsaci. The number of nematodes/500g of soil were well correlated with the number/50 g of harvested onion seeds (Seinhorst and Koert, 1971). A tolerance threshold of 2-3 nematodes/250 cm³ soil is used in Germany to indicate risk of plant infection (Knuth, 1993). D. dipsaci-infested weeds are also recognized as a potentially important inoculum source of this nematode (Gentzsch, 1973).

Seed Treatment

Chemical

Treatment of seeds with nematicides or insecticides to control seed transmission of the pathogen has had mixed success (Schiffers et al., 1984; Whitehead and Tite, 1987; Adamova and Rotrekl, 1991; Hooper, 1991). Treatment of infected garlic cloves with abamectin resulted in a 56% yield increase and eliminated all nematodes in 93% of bulbs produced (Becker, 1999) but bulbs subjected to a combination of this chemical and hot-water treatment were somewhat damaged (Jaehn and Kimoto, 1996). In the UK, the best results against the stem nematode in Narcissus were obtained when formaldehyde or peracetic acid (at 1.0 and 1.5%) were used in combination with thiabendazole (Hanks and Linfield, 1999).

Ciesla et al. (2010) suggest that methyl iodide could be used as a fumigant to eradicate D. dipsaci from alfalfa seeds. Man?asová et al. (2012) propose the use of hydrogen cyanide gas to remove D. dipsaci from seed material.

Physical

Hot-water treatments with different temperature-time combinations, depending on type and state of seed material, can be an efficient means of controlling D. dipsaci (Gratwick and Southey, 1972). Commercial cleaning of the seed has proven to be effective in removing the nematodes along with associated plant debris (Wood and Close, 1974; Neergaard, 1977).

Seed Health Tests

Sieve test (Augustin and Sikora, 1989b)

- A sample of a minimum of 300 seeds should be examined.
- The seed is submerged for 24 h in 500-1000 ml of water, insuring sufficient oxygen for the nematode mobility and survival. An extraction temperature of 10°C is the optimum for nematode extraction and simultaneously reducing turbidity of the solution.
- The nematodes in the solution are concentrated by decantation through a 25 µm sieve and are then counted.
- Microscopic examination at 1000 times magnification is necessary for correct identification of the nematode species.

Pathway Vectors

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Vector	Notes	Long Distance
Clothing, footwear and possessions	Carrying bulbs, tubers, etc	Yes
Containers and packaging - wood	Carrying bulbs, tubers, etc	Yes
Soil, sand and gravel		Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transport	Pest stages	Borne internally
Bulbs/Tubers/Corms/Rhizomes		Yes
Flowers/Inflorescences/Cones/Calyx	adults; cysts; eggs; juveniles	Yes
Fruits (inc. pods)	adults; cysts; eggs; juveniles	Yes
Leaves	adults; cysts; eggs; juveniles	Yes
Seedlings/Micropropagated plants	adults; cysts; eggs; juveniles	Yes
Stems (above ground)/Shoots/Trunks/Branches	adults; cysts; eggs; juveniles	Yes
True seeds (inc. grain)	adults; cysts; eggs; juveniles	Yes

Plant parts not known to carry the pest in trade/transport
Bark
Growing medium accompanying plants
Roots
Wood

Impact

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D. dipsaci is one of the most devastating plant-parasitic nematodes, especially in temperate regions. Without control, it can cause complete failure of host crops such as onions, garlic, cereals, legumes, strawberries and ornamental plants, especially flower bulbs.

D. dispaci is sometimes associated with other pathogens. For example, it transmits Corynebacterium insidiosum to lucerne plants (Hawn, 1963). Experimental infection of onions with D. dipsaci and Peronospora schleidenii together was 36.5% greater than with nematodes alone (Yakimenko and Efremenko, 1973).

Sturhan and Brzeski (1991) indicate that in heavy infestations, crop losses of 60-80% are not unusual. In Italy up to 60% of onion seedlings died before reaching the transplantation stage. On garlic, losses of 50% were recorded from Italy and more than 90% from France and Poland.

Diagnosis

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The development and use of a PCR method for detecting D. dipsaci in Fabaceae seeds is detailed in Kerkoud et al. (2007), and is expanded upon (with computer-assisted characterisation of ribosomal DNA) in Marek et al. (2010). A further PCR protocol is given in Kierzek et al. (2010).

A diagnostic protocol for Ditylenchus dipsaci is described in EPPO (2008).

Detection and Inspection

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D. dipsaci can be isolated from samples of suspected seed material (according to symptoms) by dissection in water at 20 times magnification. A sample of a minimum of 300 seeds should be examined. The seed is submerged for 24 hours in 500-1000 ml of water, insuring sufficient oxygen for the nematode mobility and survival. An extraction temperature of 10°C is the optimum for nematode extraction and simultaneously reducing turbidity of the solution. The nematodes in the solution are concentrated by decantation through a 25 µm sieve and are then counted (Augustin and Sikora, 1989b). Microscopic examination at 1000 times magnification is necessary for correct identification of the nematode species.

Studies have been made for species identification based on DNA probes (Palmer et al., 1991), monoclonal antibodies (Palmer et al., 1992) and restriction fragment length polymorphisms (Wendt et al., 1994). These molecular methods are very promising, but not yet used routinely. Electrophoretic techniques (Bossis et al., 1998; Tenente and Evans, 1998) and random amplified polymorphic DNA (Esquibet et al., 1998) can be used to identify populations of D. dispaci.

The species morphologically indistinguishable from D. dipsaci cannot be identified by host differentials because of the within-race variations and because some of the races freely interbreed, giving hybrids with host characteristics intermediate between those of their parents (Sturhan and Brzeski, 1991). D. dipsaci can be distinguished from D. destructor by observation of the spiculum shape (Karssen and Willemsen, 2010).

Similarities to Other Species/Conditions

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The genus Ditylenchus includes several other major nematode pests of cultures, such as D. destructor and D. angustus. D. dispaci is among the few species in this genus with median bulb well defined, 4 lines on the lateral field, stylet 10-12 µm long, and sharply pointed tail. D. ausafi has a short post-uterine sac. D. angustus has shorter spicules (less than 16 µm compared to 16-21 µm in D. dipsaci) and this species is strictly associated with rice and wild rice. In the past, D. destructor has been considered to be a synonym of D. dipsaci, but it has six lines in the lateral field.

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Cultural Control

Control by crop rotation is limited by the polyphagous habit of some races of D. dipsaci and by persistence of the nematode in clay soils but a 3-4 year rotation to lettuce eliminated the nematode in New York State (Lorbeer et al., 1997). Chemical treatments of the soil are not an economic proposition for large areas. However, it may sometimes be worth treating small patches, after lifting and destroying the affected plants (bulbs) together with a margin of surrounding healthy ones, to eradicate a slight infestation before it spreads. Systemic nematicides may be effective to some extent in controlling D. dipsaci in some ornamental crops. The use of tolerant or resistant cultivars can also reduce the damage. Nematophagous fungi such as Verticillium balanoides may be suitable for development as biological control agents for D. dipsaci (Hay and Bateson, 1997).

Soil solarization has been tried in Israel (Siti et al., 1981) and Italy (Greco et al., 1985; Greco and Brandonisio, 1990). Excellent results were seen in the Israel trials.

Sanitation

Certified nematode-free seeds and planting material are most essential to prevent crop damage by D. dipsaci. Hot-water treatments with different temperature-time combinations, depending on type and state of seed material, are operational and efficient to control D. dipsaci (Gratwick and Southey, 1972). Hot-water treatment of narcissus bulbs infected with stem nematodes consist either of storage for 1-2 weeks at 25-30°C, followed by soaking in water for 24 h and hot-water treatment at 45°C for 4 h, or storage for 1-2 weeks at 25-30°C, followed by hot-water treatment at 47°C for 4 h. Routine hot-water treatment for the control of other pests and diseases should be carried out at 43.5°C for 3 h to control any slight, possibly unnoticed nematode infection (Windrich, 1973).

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