Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Ditylenchus dipsaci
(stem and bulb nematode)

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Datasheet

Ditylenchus dipsaci (stem and bulb nematode)

Summary

  • Last modified
  • 15 July 2018
  • 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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PictureTitleCaptionCopyright
Stem and bulb nematode (Ditylenchus dipsaci); infestation of nematodes within a narcissus bulb. United Kingdom.
TitleInfestation
CaptionStem and bulb nematode (Ditylenchus dipsaci); infestation of nematodes within a narcissus bulb. United Kingdom.
Copyright©Central Science Laboratory/Harpenden Archive, British Crown/Bugwood.org - CC BY-NC 3.0 US
Stem and bulb nematode (Ditylenchus dipsaci); infestation of nematodes within a narcissus bulb. United Kingdom.
InfestationStem 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
Stem and bulb nematode (Ditylenchus dipsaci); damage to stems and bulbs on onion transplants. USA.
TitleSymptoms
CaptionStem and bulb nematode (Ditylenchus dipsaci); damage to stems and bulbs on onion transplants. USA.
Copyright©Howard F. Schwartz/Colorado State University/Bugwood.org - CC BY 3.0 US
Stem and bulb nematode (Ditylenchus dipsaci); damage to stems and bulbs on onion transplants. USA.
SymptomsStem 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
Stem and bulb nematode (Ditylenchus dipsaci); alfalfa plant showing damage due to infestation. USA.
TitleSymptoms
CaptionStem and bulb nematode (Ditylenchus dipsaci); alfalfa plant showing damage due to infestation. USA.
Copyright©Howard F. Schwartz/Colorado State University/Bugwood.org - CC BY 3.0 US
Stem and bulb nematode (Ditylenchus dipsaci); alfalfa plant showing damage due to infestation. USA.
SymptomsStem 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
Garlic bloat nematode (Ditylenchus dipsaci); nematode "wool" found between the bulbs scales of infested garlic. Cornell Plant Disease Diagnostic Clinic, Ithaca, New York, USA.
TitleInfested garlic
CaptionGarlic bloat nematode (Ditylenchus dipsaci); nematode "wool" found between the bulbs scales of infested garlic. Cornell Plant Disease Diagnostic Clinic, Ithaca, New York, USA.
Copyright©Sandra Jensen/Cornell University/Bugwood.org - CC BY-NC 3.0 US
Garlic bloat nematode (Ditylenchus dipsaci); nematode "wool" found between the bulbs scales of infested garlic. Cornell Plant Disease Diagnostic Clinic, Ithaca, New York, USA.
Infested garlicGarlic 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
Line drawing - Reproduced from Hooper DJ, 1972. CIH Descriptions of Plant-parasitic Nematodes. Set 1, No. 14. Wallingford, UK: CAB International.
TitleAdult female
CaptionLine drawing - Reproduced from Hooper DJ, 1972. CIH Descriptions of Plant-parasitic Nematodes. Set 1, No. 14. Wallingford, UK: CAB International.
Copyright©CAB International
Line drawing - Reproduced from Hooper DJ, 1972. CIH Descriptions of Plant-parasitic Nematodes. Set 1, No. 14. Wallingford, UK: CAB International.
Adult femaleLine 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

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

Notes on Taxonomy and Nomenclature

Top of page 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

Top of page 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.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ArmeniaPresentPogosyan et al., 1972; Mkrtchyan, 1983; CABI/EPPO, 2009; EPPO, 2014
AzerbaijanPresentKasimova, 1969; Kasimova and Atakishieva, 1980; CABI/EPPO, 2009; EPPO, 2014
ChinaRestricted distributionShepherd and Barker, 1990; CABI/EPPO, 2009; EPPO, 2014
-GansuPresentCABI/EPPO, 2009; EPPO, 2014
-HebeiPresentCABI/EPPO, 2009; EPPO, 2014
-HenanPresentCABI/EPPO, 2009; EPPO, 2014
-ShandongPresentCABI/EPPO, 2009; EPPO, 2014
-SichuanPresentChen, 1993; CABI/EPPO, 2009; EPPO, 2014
-XinjiangPresentWang, 1991; CABI/EPPO, 2009; EPPO, 2014
Georgia (Republic of)PresentMatveeva, 1972; CABI/EPPO, 2009; EPPO, 2014
IndiaAbsent, unreliable recordHooper, 1972; Maqbool, 1991; Sturhan and Brzeski, 1991; EPPO, 2014
-Uttar PradeshAbsent, unreliable recordLogani et al., 2002; EPPO, 2014
-West BengalAbsent, unreliable recordChakraborti, 2001
IranPresentAbivardi and Sharafeh, 1973; CABI/EPPO, 2009; Karani and Karegar, 2013; EPPO, 2014
IraqPresentStephan, 1989; CABI/EPPO, 2009; EPPO, 2014
IsraelWidespreadNevo, 1972; Siti, 1980; CABI/EPPO, 2009; EPPO, 2014
JapanPresentCABI/EPPO, 2009; EPPO, 2014
-HonshuPresentSaigusa et al., 1972; Kuroki, 1987; CABI/EPPO, 2009; EPPO, 2014
JordanPresentHashim, 1979; CABI/EPPO, 2009; EPPO, 2014
KazakhstanPresentVladimirova, 1975; German and Sagitov, 1983; CABI/EPPO, 2009; EPPO, 2014
Korea, Republic ofPresentPark SoDeuk et al., 1998; Choi, 1975; Park et al., 1993; Na SeungYong et al., 1998; CABI/EPPO, 2009; EPPO, 2014
KyrgyzstanPresentMatveeva, 1972; CABI/EPPO, 2009; EPPO, 2014
OmanPresent, few occurrences1993Al-Zidgali et al., 1994; CABI/EPPO, 2009; EPPO, 2014
PakistanPresentKhan et al., 1987; CABI/EPPO, 2009; EPPO, 2014
SyriaPresent, few occurrencesAugustin and Sikora, 1989a; Hanounik and Sikora, 1980; Akem and Bellar, 1999; CABI/EPPO, 2009; EPPO, 2014
TaiwanAbsent, invalid recordCABI/EPPO, 2009; EPPO, 2014
TurkeyRestricted distributionOkten, 1988; Enneli and Ozturk, 1989; CABI/EPPO, 2009; EPPO, 2014
UzbekistanPresentKarimova, 1973; Mavlyanov, 1973; Karimova, 1986; CABI/EPPO, 2009; EPPO, 2014
YemenPresent, few occurrencesCABI/EPPO, 2009; EPPO, 2014

Africa

AlgeriaPresentCIH, 1972; Lamberti et al., 1975; Sellami et al., 1998; CABI/EPPO, 2009; EPPO, 2014
KenyaPresent, few occurrencesCABI/EPPO, 2009; EPPO, 2014
MoroccoRestricted distributionSchluter, 1972; Andaloussi et al., 1998; CABI/EPPO, 2009; EPPO, 2014
NigeriaAbsent, unreliable recordOgbuji, 1979; EPPO, 2014
RéunionPresent, few occurrencesLamberti et al., 1986; CABI/EPPO, 2009; EPPO, 2014
South AfricaRestricted distributionLamprecht et al., 1987; Marais, 1990; CABI/EPPO, 2009; EPPO, 2014
Spain
-Canary IslandsAbsent, invalid recordEPPO, 2014
TunisiaPresent, few occurrencesHanounik et al., 1986; Kamel et al., 1989; CABI/EPPO, 2009; EPPO, 2014

North America

CanadaRestricted distributionCABI/EPPO, 2009; EPPO, 2014
-AlbertaPresentHawn, 1973; CABI/EPPO, 2009; EPPO, 2014
-British ColumbiaPresentVrain & Lalik, 1983; CABI/EPPO, 2009; EPPO, 2014
-OntarioPresentJohnson and Kayler, 1972; Fushtey and Kelly, 1975; CABI/EPPO, 2009; EPPO, 2014
-Prince Edward IslandPresentCABI/EPPO, 2009; EPPO, 2014
-QuebecPresentCABI/EPPO, 2009; EPPO, 2014
-SaskatchewanPresent, few occurrencesWatson and Shorthouse, 1979; CABI/EPPO, 2009; EPPO, 2014
MexicoWidespreadRodriguez-Chapa, 1977; Pacheco-Covarrubias, 1986; CABI/EPPO, 2009; EPPO, 2014
USAWidespreadCABI/EPPO, 2009; EPPO, 2014
-AlabamaPresentGray et al., 1980; CABI/EPPO, 2009; EPPO, 2014
-ArizonaPresentGray et al., 1976; Gray et al., 1994; CABI/EPPO, 2009; EPPO, 2014
-CaliforniaPresentViglierchio et al., 1973; Hart, 1976; CABI/EPPO, 2009; EPPO, 2014
-ColoradoPresentGray et al., 1994; CABI/EPPO, 2009; EPPO, 2014
-FloridaAbsent, invalid recordCABI/EPPO, 2009; EPPO, 2014
-HawaiiPresentCIH, 1972; Bergquist and Riedel, 1972; CABI/EPPO, 2009; EPPO, 2014
-IdahoPresentGray et al., 1994; CABI/EPPO, 2009; EPPO, 2014
-MichiganPresentHanna, 1971; Schnabelrauch et al., 1980; CABI/EPPO, 2009; EPPO, 2014
-MinnesotaPresentEPPO, 2014
-MontanaPresentGray et al., 1994; CABI/EPPO, 2009; EPPO, 2014
-NevadaPresentCABI/EPPO, 2009; EPPO, 2014
-New HampshirePresentCABI/EPPO, 2009; EPPO, 2014
-New YorkPresentChitwood and Krusberg, 1977; CABI/EPPO, 2009; EPPO, 2014
-North CarolinaPresentMuse and Muse, 1972; Chitwood and Krusberg, 1977; CABI/EPPO, 2009; EPPO, 2014
-OhioPresentTesten et al., 2014
-OregonPresentGray et al., 1994; CABI/EPPO, 2009; EPPO, 2014
-South DakotaPresentGray et al., 1994; CABI/EPPO, 2009; EPPO, 2014
-UtahPresentCampbell and Griffin, 1973; Campbell and Griffin, 1975; Gray et al., 1994; CABI/EPPO, 2009; EPPO, 2014
-VirginiaPresentMiller, 1977; CABI/EPPO, 2009; EPPO, 2014
-WashingtonPresentGray et al., 1994; CABI/EPPO, 2009; EPPO, 2014
-WyomingPresentGray et al., 1984; Franc et al., 1993; CABI/EPPO, 2009; EPPO, 2014

Central America and Caribbean

Costa RicaPresentCABI/EPPO, 2009; EPPO, 2014
Dominican RepublicRestricted distributionKermarrec and Belliard, 1977; CABI/EPPO, 2009; EPPO, 2014
HaitiRestricted distributionCABI/EPPO, 2009; EPPO, 2014

South America

ArgentinaPresent1929CIH, 1972; Mareggiani and Russo, 1992; Doucet, 1999; CABI/EPPO, 2009; EPPO, 2014
BoliviaPresentCIH, 1972; CABI/EPPO, 2009; EPPO, 2014
BrazilPresentCABI/EPPO, 2009; EPPO, 2014
-Minas GeraisPresentCharchar et al., 1980; Silva and Campos, 1991; CABI/EPPO, 2009; EPPO, 2014
-ParaibaPresentLopes and Lordello, 1980; CABI/EPPO, 2009; EPPO, 2014
-ParanaPresentSilva and Santos, 1984; Silva and Carneiro, 1992; CABI/EPPO, 2009; EPPO, 2014
-Rio Grande do SulPresentLuz, 1982; CABI/EPPO, 2009; EPPO, 2014
-Santa CatarinaPresentCharchar et al., 1980; Becker, 1993; CABI/EPPO, 2009; EPPO, 2014
-Sao PauloPresentCuri et al., 1984; CABI/EPPO, 2009; EPPO, 2014
ChileWidespreadBruna and Guinez, 1980; CABI/EPPO, 2009; EPPO, 2014
ColombiaPresentPerdomo et al., 1984; CABI/EPPO, 2009; EPPO, 2014
EcuadorRestricted distributionBridge, 1975; Bridge, 1976; CABI/EPPO, 2009; EPPO, 2014
ParaguayRestricted distributionShepherd and Barker, 1990; CABI/EPPO, 2009; EPPO, 2014
PeruPresentCIH, 1972; CABI/EPPO, 2009; EPPO, 2014
UruguayWidespreadMinagawa and Maeso-Tozzi, 1990; CABI/EPPO, 2009; EPPO, 2014
VenezuelaPresentMeredith, 1977; CABI/EPPO, 2009; EPPO, 2014

Europe

AlbaniaPresentShepherd and Barker, 1990; CABI/EPPO, 2009; EPPO, 2014
AustriaWidespread****CABI/EPPO, 2009; EPPO, 2014
BelarusPresentIvanova, 1976; Ivanova, 1984; CABI/EPPO, 2009; EPPO, 2014
BelgiumPresentClamot, 1975; Gilles et al., 1979; CABI/EPPO, 2009; EPPO, 2014
Bosnia-HercegovinaPresentKlindic et al., 1978; CABI/EPPO, 2009; EPPO, 2014
BulgariaRestricted distribution192*Zhelyazkova, 1971; Stoyanov, 1975; CABI/EPPO, 2009; EPPO, 2014
CroatiaRestricted distributionJelic, 1992; CABI/EPPO, 2009; EPPO, 2014
CyprusPresentPhilis, 1987; CABI/EPPO, 2009; EPPO, 2014
Czech RepublicWidespread****Adamova, 1975; Kudela, 1975; Baier and Balas, 1976; CABI/EPPO, 2009; EPPO, 2014
Czechoslovakia (former)PresentVlk, 1967; Branzovsky, 1973; Vinduska, 1976
DenmarkPresent, few occurrencesHansen et al., 1972; Bagger, 1976; Knuth, 1996; CABI/EPPO, 2009; EPPO, 2014
EstoniaPresent, few occurrencesKrall and Krall, 1970; CABI/EPPO, 2009; EPPO, 2014
FinlandRestricted distributionCABI/EPPO, 2009; EPPO, 2014
FranceRestricted distributionCaubel, 1973a; Caubel, 1973b; CIH, 1972; Caubel, 1972; CABI/EPPO, 2009; EPPO, 2014
-France (mainland)Restricted distributionCABI/EPPO, 2009
GermanyWidespread****Gentzsch, 1973; Homeyer, 1973; Kuthe, 1974; CABI/EPPO, 2009; EPPO, 2014
GreeceRestricted distributionCIH, 1972; Vlachopoulos, 1994; CABI/EPPO, 2009; EPPO, 2014
-Greece (mainland)Restricted distributionCABI/EPPO, 2009
HungaryRestricted distribution****Budai, 1977; CABI/EPPO, 2009; EPPO, 2014
IcelandPresent, few occurrencesSiggeirsson and Riel, 1975; CABI/EPPO, 2009; EPPO, 2014
IrelandPresent, few occurrencesCIH, 1972; Anon, 1972; CABI/EPPO, 2009; EPPO, 2014
ItalyPresentCIH, 1972; Inserra and Lamberti, 1972; Tacconi, 1972; CABI/EPPO, 2009; EPPO, 2014
-Italy (mainland)PresentCABI/EPPO, 2009
-SicilyPresentCABI/EPPO, 2009; EPPO, 2014
LatviaPresentEglitis et al., 1970; Eglitis and Kaktynya, 1972; CABI/EPPO, 2009; EPPO, 2014
LithuaniaRestricted distributionRudzyavichene Rudzeviciene, 1979; CABI/EPPO, 2009; EPPO, 2014
MacedoniaPresentKrnjaic, 1978; CABI/EPPO, 2009; EPPO, 2014
MaltaRestricted distribution1976Lamberti and Dandria, 1979; Larizza and Lamberti, 1995; CABI/EPPO, 2009; EPPO, 2014
MoldovaPresentCABI/EPPO, 2009; EPPO, 2014
NetherlandsRestricted distributionNPPO of the Netherlands, 2013; Heijbroek, 1973; CABI/EPPO, 2009; EPPO, 2014Present, in all parts of the area where host crops are grown.
NorwayPresent, few occurrencesVestad and Foss, 1971; Vestad, 1973; CABI/EPPO, 2009; EPPO, 2014
PolandRestricted distribution****Brzeski, 1972; Radziwinowicz, 1972; Kornobis and Wolny, 1997; CABI/EPPO, 2009; EPPO, 2014
PortugalRestricted distributionCarmo et al., 1974; Pereira and Santos, 1974; CABI/EPPO, 2009; EPPO, 2014
-AzoresPresentSturhan, 1973; CABI/EPPO, 2009; EPPO, 2014
-MadeiraAbsent, invalid recordEPPO, 2014
-Portugal (mainland)Restricted distributionCABI/EPPO, 2009
RomaniaRestricted distributionRomascu and Lemeni, 1972; CABI/EPPO, 2009; EPPO, 2014
Russian FederationPresentCABI/EPPO, 2009; EPPO, 2014
-Central RussiaPresentCABI/EPPO, 2009; EPPO, 2014
-Russian Far EastPresentGlotova, 1972; Matveeva, 1972; CABI/EPPO, 2009; EPPO, 2014
-SiberiaPresentMatveeva, 1972; Shpileva, 1972
-Southern RussiaPresentCABI/EPPO, 2009; EPPO, 2014
-Western SiberiaPresentCABI/EPPO, 2009; EPPO, 2014
SerbiaPresentCABI/EPPO, 2009; EPPO, 2014
SlovakiaWidespread****Valocka and Sabova, 1974; Valocka and Sabova, 1977; Liskova et al., 1988; CABI/EPPO, 2009; EPPO, 2014
SloveniaRestricted distributionCABI/EPPO, 2009; EPPO, 2014
SpainRestricted distributionAlfaro & Martinez-Beringola, 1973; CIH, 1972; CABI/EPPO, 2009; EPPO, 2014
-Spain (mainland)Restricted distributionCABI/EPPO, 2009
SwedenWidespread****Bingefors, 1973; CABI/EPPO, 2009; EPPO, 2014
SwitzerlandWidespreadNuesch, 1971; Graf and Meyer, 1973; Vallotton, 1976; CABI/EPPO, 2009; EPPO, 2014
UKWidespread****CABI/EPPO, 2009; EPPO, 2014
-England and WalesWidespreadCABI/EPPO, 2009; EPPO, 2014
-ScotlandWidespreadCABI/EPPO, 2009; EPPO, 2014
UkraineRestricted distributionMetlitskii, 1972; Shcherbak and Skarbilovich, 1973; CABI/EPPO, 2009; EPPO, 2014
Yugoslavia (Serbia and Montenegro)PresentGrujicic, 1974a; Grujicic, 1974b; Grujicic et al., 1985; Ristic et al., 1990; CABI/EPPO, 1999

Oceania

AustraliaRestricted distributionCABI/EPPO, 2009; EPPO, 2014
-New South WalesPresentAnon, 1977; CABI/EPPO, 2009; EPPO, 2014
-QueenslandPresentCABI/EPPO, 2009; EPPO, 2014
-South AustraliaPresentStirling, 1972; Dube, 1975; CABI/EPPO, 2009; EPPO, 2014
-TasmaniaPresentCABI/EPPO, 2009; EPPO, 2014
-VictoriaPresentCABI/EPPO, 2009; EPPO, 2014
-Western AustraliaPresentCABI/EPPO, 2009; EPPO, 2014
New ZealandWidespreadWilliams & Barclay, 1972; CABI/EPPO, 2009; EPPO, 2014

Risk of Introduction

Top of page 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

Top of page 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 nameFamilyContext
AlliumLiliaceaeMain
Allium cepa (onion)LiliaceaeMain
Allium cepa var. aggregatum (shallot)LiliaceaeOther
Allium porrum (leek)LiliaceaeMain
Allium sativum (garlic)LiliaceaeMain
Apium graveolens (celery)ApiaceaeOther
AstrantiaApiaceaeWild host
Avena sativa (oats)PoaceaeMain
Avena sterilis (winter wild oat)PoaceaeWild host
BegoniaBegoniaceaeMain
Bergenia (elephant-leaved saxifrage)SaxifragaceaeWild host
Beta vulgaris var. saccharifera (sugarbeet)ChenopodiaceaeMain
Brassica napus var. napus (rape)BrassicaceaeOther
Brassica rapa subsp. rapa (turnip)BrassicaceaeWild host
Cannabis sativa (hemp)CannabaceaeMain
Carduus acanthoides (Welted thistle)AsteraceaeOther
Chenopodium murale (nettleleaf goosefoot)ChenopodiaceaeWild host
Cirsium arvense (creeping thistle)AsteraceaeWild host
Convolvulus arvensis (bindweed)ConvolvulaceaeWild host
Crocus sativus (saffron)IridaceaeOther
Cucurbitaceae (cucurbits)CucurbitaceaeOther
Dianthus caryophyllus (carnation)CaryophyllaceaeOther
Fragaria ananassa (strawberry)RosaceaeMain
Gladiolus hybrids (sword lily)IridaceaeMain
Helianthus annuus (sunflower)AsteraceaeOther
Hyacinthus orientalis (hyacinth)LiliaceaeMain
Hydrangea (hydrangeas)HydrangeaceaeOther
Ipomoea batatas (sweet potato)ConvolvulaceaeOther
Lamium album (white deadnettle)LamiaceaeWild host
Lamium amplexicaule (henbit deadnettle)LamiaceaeWild host
Lamium purpureum (purple deadnettel)LamiaceaeWild host
Lens culinaris subsp. culinaris (lentil)FabaceaeOther
Medicago sativa (lucerne)FabaceaeMain
Myriophyllum verticillatum (whorled watermilfoil)HaloragidaceaeWild host
Narcissus (daffodil)LiliaceaeMain
Narcissus pseudonarcissus (wild lent lily)LiliaceaeMain
Nerine sarniensis (guernsey lily)LiliaceaeWild host
Nicotiana tabacum (tobacco)SolanaceaeMain
Onobrychis viciifolia (sainfoin)FabaceaeOther
Petroselinum crispum (parsley)ApiaceaeOther
Phaseolus (beans)FabaceaeMain
Phaseolus coccineus (runner bean)FabaceaeOther
Phlox drummondii (Annual phlox)PolemoniaceaeMain
Phlox paniculata (summer perennial phlox)PolemoniaceaeMain
Pilosella officinarum (mouse-ear hawkweed)AsteraceaeWild host
Pimpinella anisum (aniseed)ApiaceaeOther
Pisum sativum (pea)FabaceaeMain
Polyphagous (polyphagous)Main
Ranunculus arvensis (Corn buttercup)RanunculaceaeWild host
Raphanus raphanistrum (wild radish)BrassicaceaeWild host
Secale cereale (rye)PoaceaeMain
Solanum tuberosum (potato)SolanaceaeMain
Spinacia oleracea (spinach)ChenopodiaceaeOther
Stellaria media (common chickweed)CaryophyllaceaeWild host
Taraxacum officinale complex (dandelion)AsteraceaeWild host
Trifolium pratense (purple clover)FabaceaeMain
Trifolium repens (white clover)FabaceaeMain
Triticum (wheat)PoaceaeOther
Tulipa (tulip)LiliaceaeMain
Vicia faba (faba bean)FabaceaeMain
Zea mays (maize)PoaceaeMain

Growth Stages

Top of page Flowering stage, Post-harvest, Pre-emergence, Seedling stage, Vegetative growing stage

Symptoms

Top of page 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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SignLife StagesType
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

Top of page 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 enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Dactylella lysipaga Predator
Drechmeria coniospora Pathogen
Hirsutella rhossiliensis Pathogen
Rhizoglyphus echinopus Predator

Means of Movement and Dispersal

Top of page 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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VectorNotesLong DistanceLocalReferences
Clothing, footwear and possessionsCarrying bulbs, tubers, etc Yes
Containers and packaging - woodCarrying bulbs, tubers, etc Yes
Soil, sand and gravel Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
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

Top of page 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

Top of page 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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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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