Tylenchulus semipenetrans (citrus root nematode)
- Taxonomic Tree
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Natural enemies
- Notes on Natural Enemies
- Plant Trade
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Tylenchulus semipenetrans
Preferred Common Name
- citrus root nematode
International Common Names
- English: citrus nematode; root nematode
- Spanish: nematodo de la raiz de los agrios; nemátodo de las raíces; nemátodo de los cítricos
- French: anguillule des racines des agrumes; anguillule du citronnier; nématode des agrumes; nématode des citrus
- Portuguese: nematoide do citros
Local Common Names
- Germany: Nematode, Orangenwurzel-
- Italy: nematode degli agyeumi
- Japan: mikan-ne-sentyu
- TYLESE (Tylenchulus semipenetrans)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Nematoda
- Class: Secernentea
- Order: Tylenchida
- Family: Tylenchulidae
- Genus: Tylenchulus
- Species: Tylenchulus semipenetrans
DescriptionTop of page Description
The mature female has a translucent, white body, 55% or less saccate posteriorly, wide portion between excretory pore and mid body, narrowing and digitate after vulva. Annulation distinct with SEM especially in the vulval region. Lip region hemispherical, smooth, continuous with body. Framework weakly sclerotized. Stylet knobs well-developed, 3.0-3.5 µm wide. Orifice of dorsal oesophageal gland 4-6 µm behind stylet knobs. Procorpus cylindrical. Metacorpus muscular, ovoid with sclerotized valve. Isthmus elongate, surrounded by nerve ring near metacorpus. Basal bulb saccate, elongate containing three oesophageal glands. Intestine lumen indistinct. Excretory pore located 77.5-89.5% from head apex, 11.0-32.5 µm anterior to vulva and surrounded by 2-4 cuticular outgrowths. Excretory cell nucleus distinct, nucleolus prominent. Gelatinous matrix secreted through the excretory pore. Vulva slit-like, lips not sculptured. Ovary single, convoluted, extending anteriorly to metacorpus. Spermatheca, spherical, full of sperm. Uterus swollen, ovate. Rectum and anus not perceptible. Body behind vulva, digitate with smooth and round terminus. Postvulval section cavity 1.5-7.0 µm; postvulval section length 26.5-52.0 µm and postvulval section width 9.0-13.0 µm.
The male body is translucent, white, vermiform and slender. Body cuticle striae fine, 0.8-0.9 µm apart. Lateral field obscure, with two incisures. Lip region hemispherical, without distinct annulation. Labial framework inconspicuous. Stylet delicate, 9.0-10.5 µm long. Stylet knobs small, 0.5-1.0 µm wide. Orifice of dorsal oesophageal gland 4.5-6.0 µm from stylet knobs. Procorpus degenerate. Metacorpus not muscular. Isthmus cylindrical, nerve ring near metacorpus. Basal bulb distinct, pyriform, 5.0-8.0 µm wide. Excretory pore behind mid-body (54.0-68.5% of body length). Testis single occupying 24.6-36.1% of body length. Spicules slender, arcuate, 15.0-18.µm long. Gubernaculum straight or crescent-shaped, 3.0-4.0 µm long. Caudal region elongate, tapered, 34.5-44.5 µm long. Terminus rounded. Caudal alae absent.
In the female second-stage juvenile (J2), the body is translucent, white, vermiform and slightly curved when fixed. Cuticle striae 0.8 µm apart. Lateral incisures obscure, appearing as two faint lines when visible. Lip region hemispherical, not set off; labial framework weak. Stylet well-developed, 12.0-13.0 µm long (14.0 µm in some populations) with rounded knobs, 3.0-3.5 µm wide. Orifice of dorsal oesophageal gland 3.0-4.0 µm behind the stylet knobs. Procorpus cylindrical. Metacorpus muscular, ovoid. Basal bulb saccate with posterior end slightly obscured by short overlap of intestine. Deirids present, a little behind level of nerve ring. Hemizonid distinct. Excretory pore evident, located behind mid-body (52.0-57.5% of body length) and 2.0-7.0 µm anterior to genital primordium. Genital primordium with 2-4 cells, located behind mid-body (56.5-63.7% of body length). Rectum and anus visible only in live specimens; invisible in fixed specimens or in live specimens mounted in ventral or dorsal positions. Tail 55.0-70.0 µm (exceptionally 72 µm long). The nearly hyaline portion of the posterior body without fat globules >2 µm diameter, 35.0-60.0 µm long).
The male J2 can be separated from the female J2 by the presence in the posterior body of a clear, square-like area which is absent in female juveniles. The male J2 tail is <55.0 µm long compared with the female J2 tail which is >55.0 µm long.
These measurements follow Inserra et al. (1988) and are expressed in micrometres.
Mature females (N = 25); L = 389.0 (312.0-465.0); a = 4.5(3.5-6.4); b = 3.2 (2.4-4.3); stylet = 12.0 (11.0-12.5); excretory pore = 84.0 (77.7-89.8) % of body length; postvulval section cavity (PVSC) = 4.0 (1.5-7.0); postvulval section length (PVSL) = 40.0 (26.5-52.0); postvulval section width (PVSW) = 10.5 (9.0-13.0).
Males (N = 20); L = 362.0 (346.5-380.0); a = 32.1 (28.4-34.7); b = 3.4 (2.9-3.7); c = 9.0 (7.7-10.1); stylet length = 9.5 (9.0-10.5); stylet knob width = 0.8 (0.5-1.3); excretory pore = 57.1 (54.0-68.5)% of body length; spicule length = 16.5 (15.0-18.0); gubernaculum length = 3.5 (3.0-4.0); tail length = 39.5 (34.5-44.5); testis length = 113.0 (85.5-131.5).
Female second-stage juvenile (J2) (N = 20); L = 363.0 (333.5-384.5); a = 27.4 (24.8-29.1); b = 3.3 (3.0-3.7) c = 5.7 (5.4-5.9); stylet length = 12.5 (12.0-13.0); excretory pore = 54.4 (52.4-57.6)% of body length; tail length = 55.0-70.0.
Male J2 (after Van Gundy, 1958); L = 307 (284-344); stylet length = 12 (11-13).
DistributionTop of page The distribution of T. semipenetrans biotypes is not well defined. From the results of host-preference studies, it appears that the citrus biotype occurs in California and Italy (Baines et al., 1974; Inserra et al., 1980). The mediterranean biotype has been reported from countries in the Mediterranean basin and South Africa (Inserra et al., 1980; Gottlieb et al., 1986; Verdejo-Lucas, 1992). The poncirus biotype is present in California, Israel and Japan (Baines et al., 1974; Gottlieb et al., 1986). The T. semipenetrans populations from Arizona, Florida and Texas may be either citrus or mediterranean biotypes, because they infect and reproduce poorly on P. trifoliata. Their infection potential on olive trees is not known (O'Bannon et al., 1977). A resistance-breaking population of T. semipenetrans able to infect and reproduce on Swingle citrumelo (C. paradisi x P. trifoliata) and P. trifoliata has been reported in Florida (Duncan et al., 1994). The T. semipenetrans populations that occur in Argentina, Australia, Brazil, India and Venezuela may be either the citrus or mediterranean biotypes because they reproduce poorly on P. trifoliata and have not been tested on olive (O'Bannon and Ford, 1977; Campos and Barbosa Ferraz, 1980; Crozzoli and Funes, 1992).
T. semipenetrans has also been recorded in Costa Rica (Costa Rica, Boletin Cuarentenario, 1963. Nematodes found in different areas of the country by the Nematology and Vegetable Quarantine Laboratory during 1960-1963, mimeograph).
Distribution TableTop of page
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/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Afghanistan||Present||Roivainen et al., 1988; CABI/EPPO, 1999; EPPO, 2014|
|Azerbaijan||Widespread||Kasimova, 1959; CABI/EPPO, 1999; EPPO, 2014|
|Bahrain||Widespread||El-Haidari and Katcho, 1976; CABI/EPPO, 1999; EPPO, 2014|
|Brunei Darussalam||Restricted distribution||Peregrine and Younton, 1980; CABI/EPPO, 1999; EPPO, 2014|
|China||Widespread||CABI/EPPO, 1999; EPPO, 2014|
|-Anhui||Widespread||Yang & Cheng, 1987; CABI/EPPO, 1999; EPPO, 2014|
|-Fujian||Present||CABI/EPPO, 1999; EPPO, 2014|
|-Guangdong||Present||Fang, 1990; CABI/EPPO, 1999; EPPO, 2014|
|-Guizhou||Present||Jing-Mei, 1981; CABI/EPPO, 1999; EPPO, 2014|
|-Hunan||Present||Yin and Li, 1982; CABI/EPPO, 1999; EPPO, 2014|
|-Shaanxi||Present||CABI/EPPO, 1999; EPPO, 2014|
|-Sichuan||Present||CABI/EPPO, 1999; EPPO, 2014|
|Georgia (Republic of)||Widespread||Batiashvili, 1965; CABI/EPPO, 1999; EPPO, 2014|
|India||Widespread||CABI/EPPO, 1999; EPPO, 2014|
|-Andhra Pradesh||Widespread||CABI/EPPO, 1999; EPPO, 2014|
|-Assam||Widespread||Swarup, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-Delhi||Widespread||Swarup, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-Haryana||Widespread||Mukhopadhyaya and Suryanarayana, 1969; CABI/EPPO, 1999; Bajaj et al., 2012; EPPO, 2014|
|-Himachal Pradesh||Widespread||Swarup, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-Indian Punjab||Present||Swarup, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-Karnataka||Widespread||Reddy, 1977; CABI/EPPO, 1999; EPPO, 2014|
|-Kerala||Widespread||Nair, 1965; CABI/EPPO, 1999; EPPO, 2014|
|-Madhya Pradesh||Widespread||Swarup, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-Maharashtra||Widespread||Swarup, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-Rajasthan||Widespread||Swarup, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-Sikkim||Widespread||Edward & Rai, 1979; CABI/EPPO, 1999; EPPO, 2014|
|-Tamil Nadu||Present||CABI/EPPO, 1999; EPPO, 2014|
|-Uttar Pradesh||Widespread||Swarup, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-West Bengal||Present||CABI/EPPO, 1999; EPPO, 2014|
|Indonesia||Present||CABI/EPPO, 1999; EPPO, 2014|
|-Java||Widespread||Widjaja-Wisnuwardana, 1979; CABI/EPPO, 1999; EPPO, 2014|
|-Nusa Tenggara||Widespread||EPPO, 2014|
|Iran||Widespread||Abivardi et al., 1970; CABI/EPPO, 1999; EPPO, 2014; Rashidifard et al., 2015|
|Iraq||Widespread||Natour et al., 1965; CABI/EPPO, 1999; EPPO, 2014|
|Israel||Widespread||Cohn, 1965a; Cohn, 1965b; Aaronsohn, 1914; CABI/EPPO, 1999; EPPO, 2014|
|Japan||Present||CABI/EPPO, 1999; EPPO, 2014|
|-Honshu||Present||CABI/EPPO, 1999; EPPO, 2014|
|-Kyushu||Present||Nakasono et al., 1974; CABI/EPPO, 1999; EPPO, 2014|
|Jordan||Widespread||Al-Qasem and Abu-Gharbieh, 1995; CABI/EPPO, 1999; EPPO, 2014|
|Korea, Republic of||Widespread||Choi, 1975; CABI/EPPO, 1999; EPPO, 2014|
|Lebanon||Widespread||Al-Zarari and, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Malaysia||Present||CABI/EPPO, 1999; EPPO, 2014|
|Oman||Present||CABI/EPPO, 1999; EPPO, 2014|
|Pakistan||Widespread||Akhtar and Hussain, 1968; CABI/EPPO, 1999; EPPO, 2014|
|Philippines||Widespread||Davide & Dela Rosa, 1971; CABI/EPPO, 1999; EPPO, 2014|
|Saudi Arabia||Widespread||Eissa, 1976; CABI/EPPO, 1999; EPPO, 2014|
|Sri Lanka||Widespread||Macaron, 1972; CABI/EPPO, 1999; EPPO, 2014|
|Syria||Widespread||Lamberti, 1984; CABI/EPPO, 1999; EPPO, 2014|
|Taiwan||Widespread||Hung, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Thailand||Widespread||Chunram, 1972; CABI/EPPO, 1999; EPPO, 2014|
|Turkey||Widespread||Elekcioglu et al., 1994; CABI/EPPO, 1999; EPPO, 2014|
|Uzbekistan||Widespread||Tikhonova, 1957; CABI/EPPO, 1999; EPPO, 2014|
|Vietnam||Widespread||Khuong, 1983; CABI/EPPO, 1999; EPPO, 2014|
|Yemen||Present||CABI/EPPO, 1999; EPPO, 2014|
|Algeria||Widespread||Scotto La Massese et al., 1975; CABI/EPPO, 1999; EPPO, 2014|
|Central African Republic||Widespread||Luc et al., 1964; CABI/EPPO, 1999; EPPO, 2014|
|Congo||Widespread||Luc et al., 1964; CABI/EPPO, 1999; EPPO, 2014|
|Congo Democratic Republic||Widespread||De Grisse, 1971; CABI/EPPO, 1999; EPPO, 2014|
|Côte d'Ivoire||Restricted distribution||Macaron, 1972; CABI/EPPO, 1999; EPPO, 2014|
|Egypt||Widespread||Oteifa, 1955; CABI/EPPO, 1999; EPPO, 2014|
|Ethiopia||Widespread||Godrey-Sam-Aggrey et al., 1988; CABI/EPPO, 1999; EPPO, 2014|
|Guinea||Restricted distribution||Macaron, 1972; CABI/EPPO, 1999; EPPO, 2014|
|Kenya||Restricted distribution||Hollis, 1962; CABI/EPPO, 1999; EPPO, 2014|
|Libya||Widespread||Carraro, 1958; CABI/EPPO, 1999; EPPO, 2014|
|Malawi||Present||Siddiqi, 1973; CABI/EPPO, 1999; EPPO, 2014|
|Morocco||Widespread||Chapot and Delucchi, 1964; CABI/EPPO, 1999; EPPO, 2014|
|Mozambique||Widespread||Dever vd & Mangane, 1992; CABI/EPPO, 1999; EPPO, 2014|
|Nigeria||Widespread||CAVENESS, 1967; CABI/EPPO, 1999; EPPO, 2014|
|Senegal||Widespread||Taylor, 1977; CABI/EPPO, 1999; EPPO, 2014|
|South Africa||Widespread||Heyns, 1964; CABI/EPPO, 1999; EPPO, 2014|
|-Canary Islands||Present||CABI/EPPO, 1999; EPPO, 2014|
|Sudan||Widespread||Yassin et al., 1970 Plant-parasitic nematodes in Su; CABI/EPPO, 1999; EPPO, 2014|
|Tanzania||Widespread||Taylor and Ngundo, 1973; CABI/EPPO, 1999; EPPO, 2014|
|Tunisia||Widespread||Ritter, 1959; B'Chir and Kallel, 1992; CABI/EPPO, 1999; EPPO, 2014|
|Uganda||Widespread||Macaron, 1972; CABI/EPPO, 1999; EPPO, 2014|
|Zimbabwe||Widespread||Martin, 1961; CABI/EPPO, 1999; EPPO, 2014|
|Bermuda||Present||Perry et al., 1962; CABI/EPPO, 1999; EPPO, 2014|
|Mexico||Widespread||Gonzales, 1970; CABI/EPPO, 1999; EPPO, 2014|
|USA||Restricted distribution||CABI/EPPO, 1999; EPPO, 2014|
|-Arizona||Widespread||Reynolds and O'Bannon, 1963; CABI/EPPO, 1999; EPPO, 2014|
|-California||Widespread||CABI/EPPO, 1999; EPPO, 2014|
|-Florida||Widespread||CABI/EPPO, 1999; EPPO, 2014|
|-Hawaii||Present||Anderson, 1959; CABI/EPPO, 1999; EPPO, 2014|
|-Louisiana||Widespread||Fielding and Hollis, 1956; CABI/EPPO, 1999; EPPO, 2014|
|-Texas||Widespread||Godfrey, 1947; CABI/EPPO, 1999; EPPO, 2014|
Central America and Caribbean
|Belize||Present||CABI/EPPO, 1999; EPPO, 2014|
|Costa Rica||Present||CABI/EPPO, 1999; EPPO, 2014|
|Cuba||Widespread||Stoyanov, 1971; CABI/EPPO, 1999; EPPO, 2014|
|Dominica||Widespread||Anon., 1968; CABI/EPPO, 1999; EPPO, 2014|
|El Salvador||Widespread||Abrego and Tarjan, 1972; CABI/EPPO, 1999; EPPO, 2014|
|Grenada||Widespread||Edmunds, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Guadeloupe||Widespread||Scotto, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Honduras||Widespread||Pinochet et al., 1978; CABI/EPPO, 1999; EPPO, 2014|
|Jamaica||Restricted distribution||Jamaica, 1963; CABI/EPPO, 1999; EPPO, 2014|
|Martinique||Widespread||Scotto, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Panama||Widespread||Tarjan, 1967; CABI/EPPO, 1999; EPPO, 2014|
|Puerto Rico||Widespread||Ayala, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Saint Lucia||Widespread||Edmunds, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Saint Vincent and the Grenadines||Widespread||Edmunds, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Trinidad and Tobago||Widespread||Edmunds and Farrel, 1966; CABI/EPPO, 1999; EPPO, 2014|
|Argentina||Widespread||Gutierrez, 1947; CABI/EPPO, 1999; EPPO, 2014|
|Bolivia||Widespread||Tapia and Franco, 1993; CABI/EPPO, 1999; EPPO, 2014|
|Brazil||Widespread||CABI/EPPO, 1999; EPPO, 2014|
|-Bahia||Widespread||Carvalho, 1942; CABI/EPPO, 1999; EPPO, 2014|
|-Goias||Present||Martinelli et al., 2009|
|-Minas Gerais||Present||CABI/EPPO, 1999; EPPO, 2014|
|-Pernambuco||Widespread||Sharma, 1973; CABI/EPPO, 1999; EPPO, 2014|
|-Rio de Janeiro||Widespread||De Goes et al., 1982; CABI/EPPO, 1999; EPPO, 2014|
|-Sao Paulo||Widespread||Campos & Barbosa Ferraz, 1980; CABI/EPPO, 1999; EPPO, 2014|
|-Sergipe||Present||CABI/EPPO, 1999; EPPO, 2014|
|Chile||Widespread||Allen et al., 1969; CABI/EPPO, 1999; EPPO, 2014|
|Colombia||Widespread||Olivares, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Peru||Widespread||Gomez and Martin, 1967; CABI/EPPO, 1999; EPPO, 2014|
|Uruguay||Restricted distribution||Bertelli and de Bertelli, 1944; CABI/EPPO, 1999; EPPO, 2014|
|Venezuela||Widespread||Torrealba, 1969; Crozzoli and Funes, 1992; CABI/EPPO, 1999; EPPO, 2014|
|Albania||Present||CABI/EPPO, 1999; EPPO, 2014|
|Cyprus||Widespread||Philis and Siddiqi, 1976; CABI/EPPO, 1999; EPPO, 2014|
|France||Widespread||CABI/EPPO, 1999; EPPO, 2014|
|-Corsica||Widespread||Vogel, 1965; CABI/EPPO, 1999; EPPO, 2014|
|Greece||Widespread||Ayoutantis et al., 1952; CABI/EPPO, 1999; EPPO, 2014|
|-Crete||Present||CABI/EPPO, 1999; EPPO, 2014|
|Italy||Widespread||Biraghi, 1940; CABI/EPPO, 1999; EPPO, 2014|
|-Sardinia||Present||CABI/EPPO, 1999; EPPO, 2014|
|-Sicily||Present||CABI/EPPO, 1999; EPPO, 2014|
|Malta||Widespread||Lamberti & D'Andria, 1979; CABI/EPPO, 1999; EPPO, 2014|
|Portugal||Widespread||Macara, 1963; CABI/EPPO, 1999; EPPO, 2014|
|Spain||Widespread||Arias et al., 1968; CABI/EPPO, 1999; EPPO, 2014|
|Australia||Widespread||CABI/EPPO, 1999; EPPO, 2014|
|-Australian Northern Territory||Present||CABI/EPPO, 1999; EPPO, 2014|
|-New South Wales||Widespread||Anderson, 1966; CABI/EPPO, 1999; EPPO, 2014|
|-Queensland||Widespread||Colbran, 1955; CABI/EPPO, 1999; EPPO, 2014|
|-South Australia||Widespread||Meagher, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-Victoria||Widespread||Meagher, 1969; CABI/EPPO, 1999; EPPO, 2014|
|-Western Australia||Widespread||Meagher, 1969; CABI/EPPO, 1999; EPPO, 2014|
|Cook Islands||Present||CABI/EPPO, 1999; EPPO, 2014|
|Fiji||Widespread||Kirby et al., 1978; CABI/EPPO, 1999; EPPO, 2014|
|French Polynesia||Present||CABI/EPPO, 1999; EPPO, 2014|
|New Caledonia||Present||Grandison et al., 2009|
|Niue||Present||CABI/EPPO, 1999; EPPO, 2014|
|Papua New Guinea||Widespread||Bridge and Page, 1982; CABI/EPPO, 1999; EPPO, 2014|
|Samoa||Present||Orton, 1980; CABI/EPPO, 1999; EPPO, 2014|
|Tonga||Present||Orton, 1980; CABI/EPPO, 1999; EPPO, 2014|
Risk of IntroductionTop of page The risk of introducing T. semipenetrans into regions newly planted to citrus is high because the nematode has few alternative native or cultivated hosts. Therefore, phytosanitary measures which prevent the spread of the nematode should be instituted. T. semipenetrans is transported on infected planting stock, and on infested soil and equipment.
HabitatTop of page T. semipenetrans can exist in any non-temperate habitat suitable for growth of its plant hosts. In general, populations of the nematode attain higher densities in arid and mediterranean climates than in the humid subtropics or tropics (Duncan and El-Morshedy, 1996). Low, rather than high, water potentials favour population increase in heavy-textured soil (Van Gundy et al., 1962, 1964) and light-textured soil (Duncan and El-Morshedy, 1996), provided some portions of the root system have access to adequate moisture.
The presence of large amounts of organic matter increases the rate of population growth of citrus nematodes (O'Bannon, 1968). Although the population growth of T. semipenetrans is more rapid in heavy soils with moderate amounts (up to 15%) of clay and silt (Van Gundy et al., 1964; Davide, 1971; Bello et al., 1986), large numbers of nematodes can build up in sandy soils. Citrus nematodes reproduce at constant temperatures of 15-32°C, with 24-30°C being the optimum temperature and little reproduction occurring at the extremes (O'Bannon et al., 1966).
Generally, nematodes are found across the range of pH suitable for tree growth, although there is a positive relationship between population density and soil solution pH (Martin and Van Gundy, 1963; Davide, 1971; Bello et al., 1986). Saline soil conditions favour nematode population growth (Machmer, 1958). Nematode reproduction is not high when the soil solution is saline, but as the salinity declines during the rainy season, population growth is much higher on the salt-stressed plants (Mashela et al., 1992).
Hosts/Species AffectedTop of page The preferred hosts of T. semipenetrans are citrus species, although related species, such as Poncirus trifoliata and its hybrids, can be parasitized as well. Citrus nematodes also infect non-rutaceous woody plants such as grape (Raski et al., 1956), olive (Baines and Thorne, 1961), and persimmon (Raski et al., 1956; Cohn and Minz, 1961). Among grape species, Vitis berlandieri, V. riparia, V. rupestris and V. vinifera are infected by T. semipenetrans. However, these grape rootstocks differ in their reactions to different populations of T. semipenetrans (Verdejo-Lucas, 1992). Other non-rutaceous plants such as Clerodendron inerme, Garcinia mangostana and Jasminum sambac are reported as hosts of T. semipenetrans in India (Chawla et al., 1980; Bajaj et al., 1988; Nand et al., 1992).
Two more non-rutaceous hosts, Musa textilis and Cunninghamia lanceolata, have been reported in Borneo and China, respectively (Macaron, 1972; Song et al., 1994). However, the identity of these populations of T. semipenetrans needs to be confirmed. Previous reports of T. semipenetrans infection on grasses and Mikania batatifolia should be assigned to T. graminis and T. palustris (Inserra et al., 1988; Dow et al., 1990).
Owing to host differentiation, three biotypes of T. semipenetrans are recognized: citrus, mediterranean, and poncirus (Inserra et al., 1980; Gottlieb et al., 1986; Verdejo-Lucas, 1992). These biotypes share citrus species as a common host, but differ in their ability to infect and reproduce on P. trifoliata and olive. P. trifoliata is parasitized only by the poncirus biotype and olive is infected only by the citrus biotype. The mediterranean biotype reproduces poorly on P. trifoliata and does not infect olive.
(See also Geographic Distribution for discussion of biotype distribution.)
Growth StagesTop of page Flowering stage, Fruiting stage, Pre-emergence, Seedling stage, Vegetative growing stage
SymptomsTop of page The symptoms of T. semipenetrans infection on citrus trees develop slowly, and because of this, the syndrome caused by T. semipenetrans is commonly known as slow decline of citrus. The leaves of infected trees are smaller than normal and are commonly chlorotic. Wilting is more pronounced in infected trees than in healthy trees during conditions of water stress. The potassium concentration in citrus leaves and roots is inversely related to the level of nematode infection. In saline conditions, excessive sodium accumulates in the leaves of infected trees aggravating the salinity problems (Mashela et al., 1992).
A slight nematode infection may not be detected. Light infection of nursery stock is common and, in the absence of a citrus nursery certification programme, infected trees can be transplanted into citrus orchards, thus spreading the nematode.
The fibrous roots of host trees are infected by T. semipenetrans. Heavily infected fibrous roots appear thicker than healthy roots because soil particles adhere to the gelatinous egg masses of the nematode and are retained on the root surface. Infected fibrous roots decay because of the lesions and because secondary organisms infect them at the sites of nematode penetration and feeding. Heavy nematode root infections result in root lesions and cortical sloughing (Cohn, 1965b).
List of Symptoms/SignsTop of page
|Leaves / abnormal colours|
|Leaves / abnormal leaf fall|
|Leaves / wilting|
|Roots / 'dirty' roots|
|Roots / necrotic streaks or lesions|
Biology and EcologyTop of page Life Cycle
Van Gundy (1958) described the life cycle of T. semipenetrans. The nematode is an obligate parasite, which lives in modified cortical cells in the roots of a limited number of woody plants. Sedentary, swollen female T. semipenetrans are permanently attached to the fibrous roots of the host. Motile juvenile stages and males are present in the host rhizosphere.
The eggs are embedded in a gelatinous matrix surrounding the posterior portion of the female body on the surface of the host root (Cobb, 1913). As with all plant-parasitic nematodes, the first juvenile moult occurs in the egg, so that eclosion involves second-stage juveniles.
On citrus at 25°C, the female second-stage juveniles migrate along the surface of fibrous roots for up to 14 days, before feeding begins on epidermal cells. Thereafter, the juvenile moults three times until it reaches the adult stage within 7 days. Young adult females burrow the anterior portion of their bodies several cell layers deep into the root cortex and initiate the development of numerous nurse (feeding) cells around the head. At this stage, the females are sessile semi-endoparasites. The posterior portion of the female swells with maturation of the gonad. Five weeks after hatching, egg laying begins.
Males generally moult to the third stage before leaving the egg mass, and development to the adult stage can occur within 1 week without feeding. Adult males are non-parasitic.
T. semipenetrans is facultatively parthenogenetic (Van Gundy, 1958), although amphimictic reproduction generally occurs (Dalmasso et al., 1972). Five large and morphologically distinct chromosomes were found in several geographically diverse populations. Sex determination is probably heterogametic and males generally comprise 25% of the population (Dalmasso et al., 1972).
In citrus, nurse cells have single, large lobate nuclei, are highly metabolically active and function as transfer cells, providing nutrients to the female for the remainder of her life. Starch may be a major constituent of the diet of T. semipenetrans, because nurse cells contain less starch than the surrounding cells and macerated juveniles exhibit amylytic activity (Cohn, 1965a). An intricate series of intracellular exchange organelles and tubules links all the nurse cells in a feeding site with intercellular feeding tubes (B'Chir, 1988). The female can move her head to obtain access to the feeding tubes. As older nurse cells die, the females induce new cells, so that the cavity around the nematode's head becomes larger with time. This phenomenon may be partly responsible for cortical sloughing and the eventual necrosis noted on older, heavily infected roots (Cohn, 1965a).
The ecology of T. semipenetrans is influenced by its close coevolution with citrus, which has resulted in a highly developed parasitic relationship. Evidence for this intimate association is the narrow host range of the nematode, the highly developed nurse-cell structure, and the exceptionally large numbers of nematodes that can be supported by trees exhibiting only mild to moderate decline (Reynolds and O'Bannon, 1963). In contrast to Meloidogyne spp., juvenile T. semipenetrans can survive in the absence of host roots for several months to years, depending on temperature (Baines, 1950), without depleting the lipid reserves necessary for motility and infection (Van Gundy et al., 1967).
T. semipenetrans does not persist well in dry soil and population densities on drought-stressed trees decline rapidly (Tsai and Van Gundy, 1988). However, infection and population growth are rapid in localized areas of drought in the rhizosphere if other portions of the root system have adequate water (Duncan and El-Morshedy, 1996). Patterns of population change are seasonal in tropical and subtropical climates (O'Bannon et al., 1972; Toung, 1963), but seasonal change is less evident in dry or mediterranean climates (Cohn, 1966, Hamid et al., 1988). A population decline in Florida in the summer was correlated with seasonally high soil moisture and a low concentration of starch in the roots (Duncan and Eissenstat, 1993; Duncan et al., 1993).
Competition between T. semipenetrans and Pratylenchus coffeae resulted in allopatric distribution of the two species in the citrus root system in Florida (Kaplan and Timmer, 1982). In South Africa, T. semipenetrans was shown to be one of several synergistic stress factors that can cause cryptic infection of citrus roots by Fusarium solani to become pathogenic (Labuschagne et al., 1989).
Phytophthora nicotianae and P. citrophthora are the most commonly encountered plant-pathogenic fungi that infect the fibrous cortex of citrus roots concomitantly with T. semipenetrans. A recent study found that infection by the nematode reduced the concentration of P. nicotianae protein in roots and the number of fungal propagules in the soil. Moderate root infection by P. nicotianae did not appear to interfere with the life cycle of T. semipenetrans (L Duncan and J Graham, Citrus Research and Education Center, University of Florida, USA, personal communication, 1996).
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
|Bacillus thuringiensis kurstaki||Pathogen|
Notes on Natural EnemiesTop of page Nematophagous fungi, arthropods and predaceous nematodes are common inhabitants of the citrus rhizosphere in most parts of the world. In a survey of 27 orchards in Florida, 12 microbial antagonists were detected parasitizing T. semipenetrans (Walter and Kaplan, 1990). In the same survey, 29 species of nematophagous arthropods and five species of predatory nematodes were identified. Similarly, diverse communities of nematode antagonists have been reported from California (Stirling and Mankau, 1977; Imbriani and Mankau, 1983; Gaspard and Mankau, 1986). Mylonchulus sigmaturus is capable of suppressing T. semipenetrans in pots (Cohn and Mordechai, 1974). Although Pasteuria spp. are not widely reported on T. semipenetrans, they have been detected in Florida, Iraq, Iran and Italy (Fattah et al., 1989; Walter and Kaplan, 1990; Ciancio and Roccuzzo, 1992). No method of biological control is currently available for T. semipenetrans.
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Growing medium accompanying plants||adults; eggs; juveniles||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Roots||adults; eggs; juveniles||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Seedlings/Micropropagated plants||adults; eggs; juveniles||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
ImpactTop of page T. semipenetrans is a mild to moderate pathogen of citrus and grape. It appears to be economically important on grapes, primarily in California and Australia. There is no information on crop losses in other crops. T. semipenetrans is the only plant-parasitic nematode that is ubiquitous among the citrus industries of the world.
Cohn (1972) estimated annual worldwide citrus losses due to T. semipenetrans at 8.7-12.2%. The average increased fruit production as a result of managing nematode populations in heavily infested orchards varies widely, but has been consistently estimated at 15-35% (Tarjan and O'Bannon, 1974; Milne and Willers, 1979; Timmer and Davis, 1982; Childers et al., 1987; Duncan, 1989; Greco et al., 1993). Similar levels of yield loss have been estimated by determining the relationship between yield and nematode infestation levels on individual trees (Willers, 1979; Duncan et al., 1995). Crop losses due to T. semipenetrans are likely to be higher in mediterranean and dryland climates than in the humid tropics and subtropics, because nematode population densities tend to be higher in the former regions. Where citrus is marketed as fresh fruit rather than as juice, increased fruit size as a result of controlling the nematodes has been shown to be more profitable than increased yield alone (Philis, 1989).
Detection and InspectionTop of page T. semipenetrans infestations can be detected in soil and plant roots using standard nematological processing methods, including staining, Baermann funnels, soil sieving and centrifugal flotation (Southey, 1986). Specialized methods for extracting T. semipenetrans from roots have been proposed (Baines et al., 1969). Heavily infected roots may appear 'dirty' even after rinsing, because soil adheres to the gelatinous egg masses. However, the only reliable method of ascertaining the presence of T. semipenetrans and estimating its population densities is by processing soil and root samples.
Tree health is not a reliable indicator of nematode infestation. Nematode population densities are often inversely related to tree health, because of the greater root mass available on healthy trees (Reynolds and O'Bannon, 1963; Duncan and Cohn, 1990). Numerous soil factors that impair water or nutrient availability lead to symptoms similar to those caused by T. semipenetrans.
Similarities to Other Species/ConditionsTop of page The most distinctive morphological characteristics which distinguish T. semipenetrans from the other species of the genus (T. furcus, T. graminis and T. palustris) are described below.
Mature females of T. semipenetrans are less swollen (34.0-60.0% of body length) than T. furcus and T. graminis (60.0-85.1% of body length) and are similar to those of T. palustris. The postvulval section of the body of T. semipenetrans mature females is digitate with a rounded and smooth terminus, whereas that of T. furcus and T. graminis is digitate with a pointed terminus and that of T. palustris is conoid with a large base. The mature females of T. semipenetrans and T. palustris have an imperceptible rectum and anus, although these features are distinct in T. furcus and T. graminis.
Males of T. semipenetrans have a less-developed oesophagus, smaller stylet knobs (0.5-1.0 µm compared with 1.5-2.0 µm wide) and smaller basal bulb (5.0-8.0 µm compared with. 8.5-12.0 µm wide) than those of T. furcus, T graminis and T. palustris. Males of T. semipenetrans have tapered tails, like those of T. furcus and T. graminis and unlike those of T. palustris, which have cylindrical tails with a round and blunt terminus.
T. semipenetrans female second-stage juveniles (J2) have tapered tails. The tail is bifid in T. furcus J2. The rectum and anus are detectable in live J2 females of all four species. The tail of T. semipenetrans J2 female is longer (55.0-70.0 µm) than that of T. palustris J2 (42.0-54.0 µm), but does not differ from that of T. graminis (59.5-72.5 µm). In T. semipenetrans, the nearly hyaline portion of the posterior body without fat globules >2 and 3 µm is shorter (35.0-60.0 and 40.0-64.0 µm) than that of T. graminis J2 (59.0-75.0 and 64.0-78.0 µm) and does not differ from that of T. palustris (24.5-59.0 and 42.0-59.0 µm).
Prevention and ControlTop of page
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.
Soil and/or root sampling is necessary to determine the need for management tactics such as use of host-plant resistance or nematicides. In general, composite samples from beneath 12-15 trees per ha provide adequate data for management decisions. Sampling plans for citrus are available (Davis, 1984; Duncan et al., 1995). Guidelines for using nematode count data to make management decisions are available for citrus and grape, although they vary regionally (McKenry, 1982; Van Gundy, 1984; Duncan and Cohn, 1990; Le Roux, 1995). Nematode management in most regions is not thought necessary unless there are more than 1000-2000 juvenile and male nematodes per 100 cubic centimetre soil sample.
All commercially available rootstocks resistant to T. semipenetrans, such as Swingle citrumelo (Poncirus trifoliata x Citrus paradisi), are hybrids of P. trifoliata. Resistance is due primarily to a hypersensitive response to infection (Kaplan, 1981) and appears to be controlled by a single gene or several closely linked genes (Ling et al., 1994). Swingle citrumelo has good horticultural characteristics. It is reasonably cold-tolerant and is also tolerant of Phytophthora nicotianae, citrus tristeza virus, exocortis and xyloporosis viroids, and citrus blight. However, P. trifoliata hybrids are intolerant of alkaline soil, and resistant biotypes of T. semipenetrans have been reported, following widespread planting of these rootstocks (Baines et al., 1974; Duncan et al., 1994).
Early literature suggested that resistance to T. semipenetrans exists in some citranges (P. trifoliata x C. sinensis) such as Carrizo and Troyer; however, most recent work has found that these varieties are susceptible to the nematode.
Cultural practices in orchards should be evaluated before consideration is given to managing T. semipenetrans with nematicides. Water stress from drought or flooding, root infection by Phytophthora spp., high salinity and nutritional disorders may all reduce the response to T. semipenetrans management (Thomason and Caswell, 1987).
Improving sanitation is the most cost-effective method of managing T. semipenetrans (Duncan and Cohn, 1990). Using non-infected planting stock for replanting old, infested orchards can help to avoid reset problems and delay the onset of slow decline. Sanitation in newly planted orchards usually eliminates the need for future nematode management. Phytosanitary programmes are important, even in older citrus industries, because cultivated regions frequently shift in response to changes in climate, urban development and market opportunities. Additional, unquantified benefits include reduced environmental and safety problems because fewer pesticides are being used.
A fallow period before replanting old orchards infested with T. semipenetrans can reduce nematode densities to very low, often undetectable levels. Population densities remain low for several years following fallow, until canopy development provides sufficient shade to reduce the soil temperature (Reynolds and O'Bannon, 1963). Preplant fumigation can retard nematode recurrence and has been shown to be profitable when conditions favour damage by T. semipenetrans (O'Bannon and Tarjan, 1973; Le Roux, 1995).
Commercial citrus growers in Florida are legally required to purchase trees from nurseries that are certified to be free of plant-parasitic nematodes. Nursery-site approval, compliance with sanitary practices and pre-movement sampling of young trees are required for certification (Esser et al., 1988). Restricting the movement of T. semipenetrans through nursery certification was estimated to be worth an additional $32.5 million to Florida growers in 1994; the programme cost $70,000 to administer (Lehman, 1995).
Organophosphate and carbamate nematicides are currently used to manage T. semipenetrans in orchards. The best control has been achieved using split-application for these compounds, because it extends the duration of efficacy (Garabedian and Van Gundy, 1983).
How the nematicide is applied is important. A band-application of a systemic nematicide in the undercanopy of trees containing the highest density of fibrous roots and nematodes increased fruit yield compared with application along the canopy drip-line (Duncan, 1989).
Microbial degradation of some nematicides severely reduces their usefulness (Davis et al., 1993). Because of this it is desirable to reduce the nematode population to the lowest level possible, through multiple application of the most highly effective compound available.
Nematophagous fungi, arthropods and predaceous nematodes are common inhabitants of the citrus rhizosphere in most parts of the world, but no method of biological control is currently available.
ReferencesTop of page
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