Tylenchulus semipenetrans		Contents		Rev 09/14/2023
Citrus Nematode		Classification		Hosts
		Morphology and Anatomy		Life Cycle
Return to Tylenchulus Menu		Economic Importance		Damage
		Distribution		Management
Return to Tylenchulidae Menu		Feeding		References
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Classification:

     
       Tylenchina
        Criconematoidea
         Tylenchulidae
          Tylenchulinae

           Tylenchulus semipenetrans Cobb, 1913

Type species of the genus.

• First reported by J. R. Hodges in 1912 - Horticultural inspector for Los Angeles County, California.  The nematode was described by N.A. Cobb in 1913.
• Thomas at the Citrus Experiment Station (Riverside, California) reported association with poor-growing trees.
• Baines at UC Riverside worked on the use of resistant rootstocks and nematicides for 30 years.  
• Retired Dean of the College of Agriculture at University of California Riverside, Seymour Van Gundy, was hired in 1954 to work on this nematode.

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Morphology and Anatomy:

	Small nematodes, 0.25-0.35mm long.  Procorpus and metacorpus not amalgamated, distinct isthmus, postcorpus in bulb, butts intestine - distinct in juveniles (note that these features are characteristic of Criconematoidea). Females: swollen, have single ovary, vulva subterminal, eggs deposited in matrix. Excretory pore posterior (just in front of vulva). Pore surrounded by small, irregularly shaped lobes; excretory duct directed forward.  Rectum and anus atrophied or absent; non-functional.       Below:  Tylenchulus semipenetrans female dissected from a citrus root.  Photo by Ulrich Zunke.
Male:  reduced esophagus and stylet. Has no bursa. Do not feed from J2 stage onward.
Reported median body size for this species (Length mm; width micrometers; weight micrograms) - Click:

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Distribution:

Worldwide with that of citrus.  The nematode has moved around the world with transport of infested nursery stock. A low level of nematode infestation is not easily detected so that infested trees are transplanted into new orchards, thus spreading the nematode.

Occurs in 95% of citrus in California and is common in eastside San Joaquin Valley grapes, particularly in former citrus-growing areas.  

Originally spread with planting stock and further with irrigation water.

Commonly found in grape vineyards planted after citrus orchards.  Common in grape vineyards in Australia an in California vineyads with a previous history og citrus.

In Egypt, where there is expansion of citrus production in reclaimed desert areas, the danger of growing citrus seedlings infected with the citrus nematode is recognized.  Citrus yields in new plantations are threatened by nematode invasion via infected seedlings, organic fertilizers, plant materials, irrigation,, machinery, and mulching virgin soil with fertile, but probably nematode-infested, silty soil from the Nile Valley to improve soil quality.  In newly-infested areas, citrus nematode populations develop and reproduce rapidly and there are progressively greater citrus yield losses {Mahfouz et al., 2016; Scheck, 2022).    

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Economic Importance:

C-rated pest in California Nematode Pest Rating System.

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Feeding:

Ectoparasite as juvenile and young adult female, feeding on epidermal and outer cortical cells.	Sedentary semiendoparasite as mature female.  Move deeper into root as young female so  that head is near pericycle.  Establish feeding site of 8-10 nurse cells with thick walls, large nucleus and nucleolus.  The area may become invaded by other micro-organisms.   Female body outside root swells, and eggs are produced in a gelatinous matrix .
Juvenile Citrus Nematode

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Hosts:

Citrus (29 species and 21 hybrids), olive, grape, lilac, and persimmon.

Currently, there are at least four biotypes.  Biotypes are distinguished by their ability to parasitize citrus rootstocks (host range test) (Baines et al., 1974).

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Life Cycle:

Ecophysiological Parameters:

A detailed study on the life history and morphology of citrus nematode was conducted by Van Gundy (1958). Eggs are laid in a gelatinous matrix deposited by the female nematode onto the root surface. The life cycle from egg to egg takes between 6 and 8 weeks. Juveniles feed ectoparasiticaly and, as young females, penetrate the root so that the posterior end remains outside in the soil. Feeding occurs on six to ten  �nurse cells,� which are cells of the cortical endodermis around the nematode anterior regions.

Reproduction occurs over a wide range of temperatures, soil types, and pH levels (Kirkpatrick et al., 1965), with maximum population growth occurring at soil temperatures between 28 and 31 �C. Some reproduction occurs as low as 21 �C, but there is little above 31 �C.

Egg development occurs in 14 days.  After first molt in egg, J2 hatches.  Male and female J2s can be distinguished - male has a shorter esophagus and greater body diameter, with a clear area in the tail where spicules will develop.   The male passes through 3 molts without feeding, and the stylet becomes progressively less distinct; males reach maturity in one week.
Female J2s are longer and more slender.   They feed during development, initially on epidermal and outer cortical cells.  In about 21 days they molt to young females which move deeper into the root so  that the head is near the pericycle. They establish a feeding site of 8-10 nurse cells - thick walls, large nucleus and nucleolus.  The area may become invaded by micro-organisms.
Female body outside root swells, and eggs are produced in a gelatinous matrix (the soil adheres to matrix, causing a  "dirty root" symptom).
Video of Citrus Nematode Root Symptoms  >>>>
Egg mass of each female contains about 100 eggs.  When females are aggregated on a root their egg masses coalesce and cover the group. Reproduction occurs by parthenogenesis, males are not required; both male and female J2s are produced by unfertilized females.
The J2 female is the persistent stage, and has been recovered from stored soil after 2.5 years and from field soil 4 years after pulling lemon trees; however, J2 females appear susceptible to dry soil conditions, although capable of "shallow" anhydrobiosis (Tsai and Van Gundy).	In studies in California vineyards, T. semipenetrans has been found as deep as 12 feet below the soil surface.
Leachates from citrus cultivars repel T. semipenetrans, and leachates from resistant cultivars are  more repellant than those from susceptible cultivars (Duncan and Graham, 1992).   Citrus and root-knot nematodes respond differently to components of citrus root exudates (citrus is a non-host to the root-knot nematode, Meloidogyne javanica): Attractiveness and repellancy, relative to water, of components of citrus root exudates to Tylenchulus semipenetrans and Meloidogyne javanica .   Na- and K-acetate Na- and K-formate NaCl, KCl and CaCl2 Na- and K-citrate NaCO3 CO2 Citrus Roots T. semipenetrans ++++ ++ ++ -- --   +++ M. javanica -- -- --   ++ ++ -- Greatest aggregation of T. semipenetrans was at 0.08-0.10 M Na-acetate. Above 0.2 M recovery was very low. Preference for Na-acetate by T. semipenetrans was pH-dependent. [Data from Duncan et al (1993) and Abou-Setta and Duncan (1998)] Duncan and Abou-Setta (1995) used the attractiveness of acetates to attract citrus nematode into soil zones with high concentrations of  nematicides or bacterial antagonists.
Reproduction of citrus nematode in the upper soil was greater when only lower soil levels were irrigated than when the soil was uniformly moist or uniformly dry. Why?  Some possibilities: hydraulic lift of water from the lower soil to the nematode-infested regions of the root accessible to the sedentary endoparasite females. availability of O2 to the reproducing females. unfavorable soil conditions for biological antagonists. combinations of all these factors. Research by Duncan and El-Morshedy (1996)   Duncan (personal communication) considers that soil moisture may be the most important factor regulating populations of this nematode.  He notes that population densities and crop losses associated with citrus nematode are higher in dryland or Mediterranean citrus production than in the humid tropics and subtropics.  Also, he notes that the host range of the citrus nematode is limited to a few deep- rooted perennials so there may not have been selection pressure for anhydrobiosis.

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Damage:

Infected plants exhibit debilitating slow decline, small leaves, twig die- back, reduced foliage, reduced fruit size and number.	Infected feeder roots (left) are stunted and have clinging soil particles; healthy roots on right.		Growth reduction in citrus trees planted in an old orchard. Row on right preplant fumigated with 1,3-D nematicide.
		Mature female Tylenchulus semipenetrans dissected from root.  Distortion of anterior region caused by constriction by host cell walls.

Root destruction causes plant decline over 3-5 years.  

Nematodes occur in very high numbers.  Scotto la Massese in France estimates a 5% yield loss per 1,000 nematodes per g of root.  In Israel, tree performance is reduced at levels of > 40,000 nematodes per 10g of root.

Mashela, Duncan et al, 1992, showed that feeding of T. semipenetrans changed the partitioning of osmoticum ions in citrus: K decreased in  leaves; K⁺, Na⁺, and Cl^- decreased in roots, and Cl^- increased in leaves.

Leaf symptoms in citrus are consistent with the increased Cl^- concentrations.  Starch concentrations increased in infected roots.
   

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Management:

Avoidance - clean planting stock, use of certified material, bare root dips in hot water (45 C for 25 minutes) effective.

Prevent spread - give attention to machinery, planting stock, and irrigation water. Certification and regulatory programs are important to reduce spread into new areas of citrus production (Mahfouz et al., 2016).

Nematicides

Pretreatment 4-8 months before planting with 1,3-Dichloropropene (1,3-D) at 70-120 gpa placed 12-24" deep at 18" spacing reduces, but does not eradicate nematode populations.  Can also use tarped methyl bromide at 100-200 lb/acre 1  month before planting.  

Effect of preplant soil fumigation with 1,3-Dichloropropene (1,3-D) exhibited in 4-year old navel orange trees:

Untreated control	Preplant fumigation at 50 liters/ha

Prior to 1979, DBCP was used postplant at 34-36 lb/acre, but not for the first 4 years, and then not more than once every 3 years.

Commercial microbial antagonist formulations performed poorly against Tylenchulus semipenetrans and Paratrichodorus lobatus compared to the nematicides Aldicarb, cadusafos and metalaxyl:

• Prosper Nema did not reduce nematode levels even when combined with a sawdust mulch over the soil. 
• Nutri-life 3/20 inhibited citrus growth and caused leaf chlorosis. 
• Potassium silicate reduced levels of T. semipenetrans in soil. 
• Cadusafos and Aldicarb were equally effective in controlling T. semipenetrans on roots but cadusafos was more effective in soil. 
• Relatively low initial combined levels of T. semipenetrans and Paratrichodorus lobatus depressed citrus growth
• Cadusafos (3 applications at 3 g/m2 over 6 months) reduced T. semipenetrans to very low levels, but did not eliminate the nematode; mechanical incorporation of nematicide granules improved the level of nematode control after the first, but not succeeding, applications (Walker and Morey, 1999a)

Green Manures:

Brassica cultivars Ebony and Indian mustards, and Rangi rape residues reduced the soil level of Tylenchulus semipenetrans by up to 76% compared with unamended soil, and in a greenhouse reduced levels on the roots of orange (Citrus sinensis) seedlings. 

Paratrichodorus lobatus reached high levels in pots containing unamended soil but was not detected in pots containing amended soils. 

In field experiments brassica cultivars were grown in orchards (20 kg seed/ha) as green manure crops.  Although soil levels of T. semipenetrans were reduced by 79-91% by incorporation of green manures, brassica cultivars including Ebony, Indian and Yellow mustards, and Humus and Rangi rapes, were no more effective than were self-seeding weeds. Growth of citrus did not differ between soils amended with brassica or weed residues (Walker and Morey, 1999b).

Resistant rootstocks

• Poncirus trifoliata - trifoliate rootstock.
• Troyer citrange - but biotypes pose a threat.

When tested against a Mediterranean biotype, all selections with 'Troyer' citrange (Citrus sinensis X P. trifoliata) in their parentage supported nematode reproduction. (Verdejo et al, 2000).

Citrus hybrid rootstocks were tested against a Mediterranean biotype of Tylenchulus semipenetrans. Seven selections of the cross 'Cleopatra' mandarin (Citrus reshni X Poncirus trifoliata), and one of Citrus volkameriana X P. trifoliata were highly resistant to the citrus nematode and did not support nematode reproduction. The nematode showed very low infectivity and reproductive potential on seven additional selections of 'Cleopatra' mandarin X P. trifoliata, one of 'King' mandarin x P. trifoliata, and two C. volkameriana X P. trifoliata. These selections were considered nematode resistant (Verdejo et al, 2000).

The resistant response of Carrizo citrange resistant rootstock:  Necrotic tissue and wound periderm surrounding head of invading young female.

Host Plant Resistance, Non-hosts and Crop Rotation alternatives:

Additional Information and Resources

Australasian Plant Pathology Society Factsheets on Plant-parasitic Nematodes (Prepared by Dr. Graham R. Stirling)

(Use your Return Key or click the Index Tab to return to this Nemaplex page)

• PSN 032. Citrus nematode (Tylenchulus semipenetrans), the cause of slow decline of citrus

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References:   

Abou-Setta, M. M.; Duncan, L. W. 1998.  Attraction of Tylenchulus semipenetrans and Meloidogyne javanica to salts in vitro. Nematropica 28: 49-59.

Baines, R. C., Cameron, J. W., and Soost, R. K. 1974. Four biotypes of Tylenchulus semipenetrans in California identified, and their importance in the development of resistant citrus rootstocks. Journal of Nematology, 6, 63�66.

Chitambar, J. J., Westerdahl, B. B., and Subbotin, S. A. 2018. Plant Parasitic Nematodes in California Agriculture. In Subbotin, S., Chitambar J., (eds) Plant Parasitic Nematodes in Sustainable Agriculture of North America. Sustainability in Plant and Crop Protection. Springer, Cham.

Verdejo-Lucas, S.; Sorribas, F. J.; Forner, J. B.; Alcaide, A. 2000.  Resistance of hybrid citrus rootstocks to a Mediterranean biotype of Tylenchulus semipenetrans Cobb. Hortscience 35: 269-273.

Walker, G. E.; Morey, B. G. 1999a.  Effects of chemicals and microbial antagonists on nematodes and fungal pathogens of citrus roots. Australian Journal of Experimental Agriculture 39: 629-637.

Walker, G. E.; Morey, B. G. 1999b.  Effect of brassica and weed manures on abundance of Tylenchulus semipenetrans and fungi in citrus orchard soil. Australian Journal of Experimental Agriculture 39: 65-72.

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Copyright © 1999 by Howard Ferris.
Revised: September 14, 2023.