Ditylenchus angustus
(rice stem nematode)

Pictures

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Identity

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Preferred Scientific Name

• Ditylenchus angustus (Butler, 1913) Filipjev, 1936

Preferred Common Name

• rice stem nematode

Other Scientific Names

• Anguillulina angusta (Butler, 1913) Goodey, 1932
• Tylenchus angustus Butler, 1913

International Common Names

• English: ufra disease
• Spanish: nemátodo del tallo del arroz
• French: nématode de la tige du riz

Local Common Names

• India: dak pora
• Myanmar: akhet-pet
• Vietnam: tiem dot san

EPPO code

• DITYAN (Ditylenchus angustus)

Taxonomic Tree

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

Description

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Measurements From Rice at Joydevpur, Bangladesh (Seshadri & Dasgupta, 1975) 15 females: L = 0.8-1.20 mm; a = 50-62; b = 6-9; c = 18-24; V = 78-80; stylet = 10-11 µm. 10 males: L = 0.7-1.18 mm; a = 40-55; b = 6-8; c = 19-26; T = 60-73; spicules = 16-21 µm; gubernaculum = 6-9 µm; stylet = 10 µm. 6 juveniles: L = 0.5-0.7 mm; a = 41-60; b = 6-9; c= 14-18; stylet = 8-10 µm. From Type Host and Locality (after Butler, 1913) females: L = 0.7-1.1 (0.9) mm; a = 47-58 (50); width= 15-22 (19 µm); b = 7.0 (?); c = 15-23 (20); V = 70-80; stylet = 9 or 10 µm. eggs = 80-88 µm x 16-20 µm. males: L = 0.6-1.1 mm; a = 36-47 (44); width = 14-19 µm; b = 7 (?); c = 18-23; stylet = 9 or 10 µm. After Goodey, 1932 females: L = 0.7-1.23 mm; a = 36-58; b = 7-8; c = 17-20; V = 80; stylet = 10 µm. males: L = 0.6-1.1 mm; a = 36-47; b = 6-7; c = 18-23; stylet = 10 µm. Description (after Seshadri and Dasgupta, 1975) Female Body slender, almost straight to slightly arcuate ventrally when relaxed by application of gentle heat. Cuticle with fine transverse striations; annules about 1 µm wide at mid-body. Lip region unstriated, not distinctly set off from the body, low, flattened, wider than high at lip base. Cephalic framework lightly sclerotized, hexaradiate, en-face view showing six lips of almost equal size. Lateral fields one-fourth of body width or slightly less, with 4 incisures, outer incisures more distinct than inner ones, extending almost to tip of tail. Deirids immediately posterior to the level of excretory pore. Phasmids close behind mid-part of tail, pore-like, difficult to see. Stylet moderately developed, conus attenuated, about 45% of total stylet length; knobs small but distinct, usually with posteriorly sloping anterior surfaces, rather amalgamated with one another, about 2 µm across. Procorpus cylindrical, narrows as it joins median oesophageal bulb, as long as 3-3.6 times body-width in that region. Median oesophageal bulb oval, with a distinct valvular apparatus anterior to the centre. Isthmus narrow, cylindrical, 1.5 to 1.9 times as long as procorpus; posterior oesophageal bulb usually clavate; 27-34 µm long, slightly overlapping the intestine, mainly on the ventral side, with 3 distinct gland nuclei. Cardia absent. Nerve ring conspicuous, 21-35 µm behind median oesophageal bulb. Excretory pore 90-110 µm from anterior end, slightly anterior to beginning of posterior oesophageal bulb. Hemizonid 3-6 µm anterior to excretory pore. Vulva a transverse slit, vaginal tube somewhat oblique, reaching more than half-way across body. Spermatheca very elongated, packed with large, rounded sperms. Anterior ovary outstretched, oocytes in single row, rarely in double rows. Post-uterine sac collapsed, without sperms, 2.0-2.5 times as long as vulval body width, extending about 1/2 to 2/3 distance to anus. Tail conoid, 5.2 to 5.4 times the anal body width in length, tapering to a sharply pointed terminus resembling a mucro. Male As numerous as females. Body almost straight to slightly curved ventrally when fixed. Morphology similar to females. Caudal alae (bursa) present, narrow in some specimens, beginning opposite the proximal end of spicules, extending almost to tail tip. Spicules curved ventrally, simple; gubernaculum short, simple. Juveniles Similar to adults in gross morphology, oesophagus proportionally longer than in adults. Additional morphological and morphometric data was provided by Mian and Latif (1995). Type Host and Locality Oryza sativa, in Eastern Bengal (= Bangladesh).

Debanand Das and Bajaj (2008) provide a redescription of D. angustus based on specimens collected from flooded rice from Assam, India. The specimens were morphologically distinct from previously described specimens, having head shape, narrow and slender isthmus, crustaformeria with four to five cells in each row, longer post-vulval uterine sac, and short conoid tail with a mucro.

Distribution

Top of page Jack (1923) mentioned D. angustus as a parasite of rice in Malaya, but Rahim (1988) noted its absence from samples from Peninsular Malaysia. Vuong (1969) described D. angustus as a serious problem in Madagascar, but this has not been confirmed more recently.

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.

Risk of Introduction

Top of page Risk Criteria Category

Economic Importance Low
Distribution Africa, Asia
Seedborne Incidence Low
Seed Transmitted Yes
Seed Treatment Yes

Overall Risk Low

Notes on phytosanitary risk

Locally, D. angustus could be spread in infested soil and plant material. The risk of international seedborne dispersal in dried seed is not significant.

Habitat

Top of page D. angustus parasitizes wild and cultivated species of Oryza in the major river deltas of South and South-East Asia. These areas are prone to deep or very deep flooding during the rainy season. Shallower flooded, irrigated lowland rice within these areas is also parasitized in the dry season. Rice crops in upland areas are not parasitized.

Hosts/Species Affected

Top of page The host range of D. angustus is usually confined to Oryza spp., including rice and wild species. Leersia hexandra has been recorded as a host in Madagascar (quoted in Seshadri and Dasgupta, 1975).

Host Plants and Other Plants Affected

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Growth Stages

Top of page Seedling stage, Vegetative growing stage

Symptoms

Top of page During vegetative growth from seedling to flag leaf, the principal symptom of infection is leaf chlorosis. In light infections, the chlorosis will be discrete white spots, less than 1 mm in diameter. As nematode numbers increase, these spots become more numerous, intensify and coalesce towards the base of the penultimate leaf and lower part of the emerging leaf. D. angustus does feed on the inner surface of the leaf sheaths, but these rarely show obvious symptoms. In time the chlorotic areas will show some localized browning.

Depending on the severity of infection, chlorotic leaf areas, tillers or whole plants will wither and die, attaining a light-brown appearance. In severe infections, the entire crop takes on this appearance.

If infected tillers survive to flowering then the panicles remain partially or completely enclosed within the leaf sheath. Partially emerged panicles bear few, if any, true seed and the empty spikelets are distorted and discoloured.

List of Symptoms/Signs

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Biology and Ecology

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D. angustus survives between crops in an anhydrobiotic state in rice stem tissues and in partially or fully enclosed panicles (Cox and Rahman, 1979; Kinh, 1981). D. angustus is dependent on environmental conditions to survive dehydration (Ibrahim and Perry, 1993) and successful anhydrobiosis relies on slow drying, which occurs, for example, in dry soil (Cuc, 1982) or within plant tissues. Butler (1913) recovered nematodes after 7-15 months from plant material. D. angustus can be present in freshly harvested mature true seed and in sterile spikelets (Butler, 1919; Hashioka, 1963; Cuc and Giang, 1982; Ibrahim and Perry, 1993) and although transmission in seed can occur (Sein, 1977a), the risk of such transmission is minimal, particularly after thorough sun drying (Seshadri and Dasgupta, 1975). The anhydrobiotic population is predominantly fourth-stage juveniles (Ibrahim and Perry, 1993): this stage has the greatest infective and reproductive potential (Plowright and Gill, 1994).

Nematodes are spread in water or by leaf contact at high relative humidities (>75% RH) (Rahman and Evans, 1987); long-distance spread in water is possible (Bridge et al., 1990). D. angustus invades rice plants at the water surface (Plowright and Gill, 1994) and rapidly enters the innermost leaf interstices, where it feeds on meristematic tissues and on young leaves within the leaf sheath. Young plants are more easily invaded than old (Rahman and Evans, 1987). It has a short life cycle, 10-20 days at 30°C, and populations tend to have a stable demographic equilibrium in which fourth-stage juveniles predominate (Plowright and Gill, 1994).

Seedborne Aspects

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Incidence

Prasad and Varaprasad (2002) have shown that D. angustus is seedborne. The nematode was found infecting irrigated rice in Godavari delta, India, which is located away from the ufra endemic zone (Assam, india). Live nematodes were recovered from the dried seeds, mainly located in the germ portion, 3 months after harvest. D. angustus can be present in freshly harvested, mature, true rice seed and in sterile spikelets (Butler, 1919; Hashioka, 1963; Sein, 1977a; Cuc and Giang, 1982; Ibrahim and Perry, 1993). In Burma, rice plants heavily infested with D. angustus produced panicles containing many unfilled grains. An average of 15.4 nematodes was found in each unfilled 'grain' compared with 5.3 in mature grain. The desiccation survival of third- and fourth-stage juveniles and adults of D. angustus was examined at different relative humidities on glass slides, on agar and agarose substrates, and in infested rice stems and seeds. Individual nematodes show no intrinsic ability to control water loss and survive severe desiccation. Nematodes of all three stages are dependent on high humidities and/or protection by plant tissue for long-term survival (Ibrahim and Perry, 1993). In another study, 2-day-old seeds of rice varieties Nep mua and Lua Tieu infested with D. angustus at 16.5-17% RH had 7 and 63 nematodes per 100 unfilled grains, and 25 and 167 nematodes per 100 filled grains, respectively. When infested seeds were dried in the sun (44-45°C) for 4 days (6 h/day), seed humidity decreased to below 12% and the nematodes were killed (Cuc and Giang, 1982).

Seed Transmission

When naturally infected seeds were used as an inoculum source, large numbers of seeds grown together resulted in diseased plants (Sein, 1977a). However, the risk of such transmission is minimal, particularly after thorough sun drying (Seshadri and Dasgupta, 1975).

Seed Treatments

Soaking rice seed for 24 hours in thiabendazole (0.1%) or ethylthiocyanoacetate (0.13%) was effective and economically feasible for control of D. angustus (Vuong Huu Hai and Rodriguez, 1972). Chakraborti (2000) tested a variety of treatments to rice seeds or seedlings for control of rice stem nematode and found that using a trap crop (cv. Shalibahan) in the seed bed combined with the application of azadirachtin and neem (Azadirachta indica) oil to seedlings for 30 minutes gave the lowest mean percentage of infected tillers (1.8 per 25 hills) and nematode population (12.3 per 250 g of soil) and the highest yield (3.0 t/ha). Other treatment combinations or individual treatments also effectively suppressed the nematodes, but some were only as efficient as the control. Rahman (1996) examined the management of ufra disease, caused by D. angustus, with or without stubble cleaning, ZnSO4, neem cake and neem seed dust in transplanted Aman and irrigated Boro rice. Neem seed dust controlled ufra disease with 72.2-91.0% healthy panicles producing 5.3 to 6.7 t/ha yield. Simple stubble cleaning had less ufra infestation and produced two to three times more yield than the control (diseased) and no stubble cleaning treatments.

Pathway Vectors

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Plant Trade

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

Impact

Top of page D. angustus has a limited geographical distribution and it is solely a pest of rice, although it does occur on different types of flooded rice from deepwater to lowland irrigated. It has been recorded and confirmed on rice from India, Bangladesh, Thailand, Myanmar and Vietnam. There are also individual reports of it occurring in the Philippines, Indonesia, Pakistan, Madagascar, Malaysia, Egypt and Sudan but there has not been confirmation of these reports nor any information on the economic importance of the nematode in these countries.

D. angustus was first found and described in northern India on deepwater rice and early observations reported 50% yield losses of rice in Uttar Pradesh (Singh and Garg, 1949; Singh, 1953; Prasad et al., 1987). It occurs in 20-80% of rice in West Bengal (Chakrabarti et al., 1985). In India, rice yield losses have been estimated to range from 10 to 15% in West Bengal and 30% in Assam (Rao et al., 1986; Prasad et al., 1987).

As D. angustus has very specific environmental requirements mainly related to humidity and rainfall, it is very localized and often does not even occur in the same rice fields each year (Bridge et al., 1990). It has been, for example, most severe in the wettest years and wettest areas of Bangladesh (Cox and Rahman, 1980) and in Vietnam, the damage has been the most severe in months of high rainfall or in fields with high water levels (Cuc and Kinh, 1981). When deepwater rice was more widely grown in Bangladesh, it was estimated that there was an annual yield loss of 20% over 20% of the rice-growing area, equal to 4% yield loss overall (Catling et al., 1979). However, when it does occur, it is one of the most devastating of rice diseases (Cox and Rahman, 1980) and can cause complete crop failure.

It has been known as a serious pest of rice in Thailand where in 1963 it was estimated that 500 ha of lowland rice had yield losses ranging from 20 to 90% caused by D. angustus (Hashioka, 1963). Similarly in Vietnam in the Mekong Delta during 1974 it caused total yield loss of hundreds of hectares of deepwater rice in one Province and in 1982 up to 100,000 ha of rice in the Delta were affected by D. angustus (Cuc and Kinh, 1981; Catling and Puckridge, 1984; Bridge et al., 1990). By 1987 in Bangladesh about 200,000 ha or 60-70% of flooded rice areas were infested with the nematode (Mondal and Miah, 1987).

The economic impact of D. angustus has been influenced over the past 10 to 15 years by shifts in the crops favoured by farmers in deepwater rice areas. Areas previously sown to deepwater rice in Vietnam and Bangladesh have seen the progressive abandonment of the crop in favour of lowland crops through the introduction of high-vielding varieties and the development of irrigation facilities for dry-season rice. As the total deepwater rice area has reduced, so the area infested by D. angustus has also declined. In recent surveys, less than 1000 ha of rice in three provinces in Vietnam were infested (Cuc and Prot, 1992). Recent surveys in Bangladesh have found infestations in only 1500 ha of deepwater rice in nine districts (ML Rahman, Bangladesh Rice Research Institute, Joydebpur, Dacca, Bangladesh, personal communication, 1994), equivalent to <1% of the crop area. The distribution of D. angustus in Thailand is also becoming more restricted (Prot, 1993).

In Bangladesh, however, D. angustus has become established in lowland rice (Miah and Rahman, 1985). Lowland rice in 14 low-lying districts of South Bangladesh was infested in 1993. In Gazipur, 33-100% of fields sampled were infested and crop loss estimates were 17-57% (Plowright et al., 1995). Complete crop failure occurred in some fields within the infested area.

Detection and Inspection

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D. angustus feeds on tissue developing within the leaf sheath, so the youngest emerging leaf should be examined for symptoms in the field. Symptoms will develop within 1-3 weeks of infection, depending on the size and source of the initial inoculum. Infected plant residues, before flooding, provide primary infection sources in a field, whilst secondary and tertiary infection occurs from water with the onset of flooding.

Symptoms of low infection are difficult to detect: to accurately assess or confirm infection it is therefore necessary to sample tillers in the field. Tillers should be cut above the peduncle because nematodes are not found in the internodes below the growing point. 1-cm sections of the leaf sheath should be split longitudinally and placed in water for 24 h on a Baermann funnel placed in a bijou bottle or similar vessel. The nematodes will migrate into the water and can then be collected and counted. Such extracts may become foul within 24 h. For immediate examination of samples, leaf sheaths can be teased apart in water in a Petri dish to release nematodes and observe directly.

Similarities to Other Species/Conditions

Top of page D. angustus is very similar to other species of the genus, but none of these are pests of rice.

It is also similar in general appearance to Aphelenchoides besseyi, the cause of white tip disease of rice, particularly under the dissecting microscope. The females and juveniles of the species are very similar under low-power microscopy, although they can be distinguished by the more experienced nematologist using characters such as head shape and form of the oesophageal bulb. The males are more easily distinguished as the tail shape, spicule shape and presence or abundance of bursa are easier to see. Ideally, identification should be confirmed by a competent taxonomist.

PCR studies using a fragment of ribosomal DNA have also been used to separate D. angustus from species of Aphelenchoides (Ibrahim et al., 1995).

Prevention and Control

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Introduction

The Deepwater Rice Management Project (Anon., 1987) listed control measures which may be appropriate against D. angustus:

- thorough burning of crop residues to eliminate all infested stem terminals

- extending the overwintering period by delayed planting

- the use of shorter-duration cultivars

The use of resistant cultivars, when they become available, should prove to be the most effective measure.

Cultural Control

Burning of infested crop residues gives very effective control and has long been advocated (Butler, 1919). Thorough burning is essential, although it is not always possible where soil remains water-logged after harvest or when a large proportion of the straw is removed for other purposes (e.g. for cattle fodder), leaving insufficient for effective burning (McGeachie and Rahman, 1983).

Ploughing in crop residues can reduce ufra (caused by D. angustus) because nematodes decline more rapidly in moist soil than in foliar remains (Butler, 1919). This is not always possible and depends on local circumstances and soil conditions.

Growing a non-host crop, such as jute, in rotation with deepwater rice can reduce the incidence of ufra in fields where the rise of floodwater is not excessively fast (McGeachie and Rahman, 1983). Lowland transplanted rice rotated with a non-host, mustard, was less affected by ufra than continuously cultivated rice (Miah and Rahman, 1985).

Removal of volunteer and ratoon rice plants, wild rice and other host weeds will help prevent the carryover between seasons, and banks between plots may also be beneficial (Sein and Zan, 1977).

D. angustus survives for a limited period: lengthening the overwintering period can reduce primary infection (Cox and Rahman, 1980; McGeachie and Rahman, 1983). This can be achieved with deepwater rice by using short-duration cultivars (which would reduce population densities of the nematode at harvest) or by late sowing and transplanting. Manipulation of rice cropping patterns and cultivation techniques is a promising means of control (McGeachie and Rahman, 1983).

Where it is possible, submerging young seedlings for a week would reduce infection in lowland rice. Maintaining water levels well below the top of the leaf-sheath collar throughout the crop in lowland rice reduces nematode dispersal and secondary and tertiary infection. It is essential to protect seedlings (that are in seed beds and destined to be transplanted) from early infection, especially for the first 14 days after sowing.

Rahman (1996) reported upon ufra disease management in rainfed lowland and irrigated rice in Bangladesh. Rahman (1996) found that neem seed dust was effective in controlling ufra disease. Stubble cleaning was also effective at reducing infection.

Host-Plant Resistance

A large number of deepwater and lowland rice cultivars have been tested against D. angustus.

In Vietnam, four high-yielding, local improved breeding lines (IR9129-393-3-1-2, IR9129-169-3-2-2, IR9224-117-2-3-1, IR2307-247-2-2-3) and three cultivars (BKN6986-8, CNL53, Jalaj) are described as slightly infected (Kinh and Phuong, 1981; Kinh and Nghiem, 1982). A Burmese cultivar (B-69-1) from the Irawaddy Delta was tolerant of ufra disease (Sein, 1977b), and a Thailand cultivar (Khao Tah Ooh) was relatively less susceptible (Hashioka, 1963). Two cultivars in West Bengal, India (IR36 and IET4094) were also less susceptible (Chakrabarti et al., 1985). Complete resistance to D. angustus has been found in wild rice, Oryza subulata, and a deepwater cultivar, RD-16-06 (Miah and Bakr, 1977a). The Rayada group lines are highly resistant to D. angustus in Bangladesh, and others showing moderate resistance are CNL-319, BR306-B-3-2, BR308-B-2-2, Bazail 65 and Dalkatra (Rahman, 1987). Improved cultivars could become available to farmers in the near future (Anon., 1987).

The cultivars Padmapani and Digha are not attacked by D. angustus in areas of India and Bangladesh. It is suggested that they escape the disease because of their short growth duration (Mondal and Miah, 1987; Rathaiah and Das, 1987).

Plowright et al. (1996) recorded the induction of phenolic compounds in rice after infection by D. angustus. Chlorogenic acid occurred in small quantities and was only found in resistant plants. Levels increased in response to infection. Sakuranetin, a phytoalexin, was isolated from two resistant selections of Rayada 16-06. There was correlative evidence that the compound had a functional role in resistance.

Das and Sarmah (1995) claimed 80% resistance or more to D. angustus in RDA 14, RDA 4, RDA 2, RDA B4, RDA 16-06/1/2, RDA B8, RDA 3, Bazail 65, RDA B5 and RDA B3 genotypes. The resistance was expressed in field trials in Assam.

Sarma et al. (1999), working in Assam, evaluated 19 advanced breeding lines from Bangladesh. Three resistant lines were recommended for deeply flooded areas of Assam while the remaining lines may be more suitable for less flooded areas.
 

References

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