Aphelenchoides besseyi (rice leaf nematode)
Index
- Pictures
- Identity
- Taxonomic Tree
- Description
- Distribution
- Distribution Table
- Risk of Introduction
- Habitat
- Host Plants and Other Plants Affected
- Growth Stages
- Symptoms
- List of Symptoms/Signs
- Biology and Ecology
- Natural enemies
- Seedborne Aspects
- Pathway Vectors
- Plant Trade
- Impact
- Diagnosis
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- References
- Distribution Maps
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Top of pageIdentity
Top of pagePreferred Scientific Name
- Aphelenchoides besseyi Christie 1942
Preferred Common Name
- rice leaf nematode
Other Scientific Names
- Aphelenchoides oryzae Yokoo 1948
- Asteroaphelenchoides besseyi (Christie 1942) Drozdovski 1967
International Common Names
- English: summer crimp nematode; white tip; white tip nematode of rice
- Spanish: nematodo de la punta blanca del arroz
- French: nématode du bout blanc du riz; nématode foliaire du riz
EPPO code
- APLOBE (Aphelenchoides besseyi)
Taxonomic Tree
Top of page- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Nematoda
- Order: Aphelenchida
- Family: Aphelenchoididae
- Genus: Aphelenchoides
- Species: Aphelenchoides besseyi
Description
Top of page(from type host and locality after Christie, 1942):
* 10 females: L = 0.66-0.75 mm; a = 32-42 (width = 17-22 µm): b = 10.2-11.4 (oesophagus = 64-68 µm): c = 17-21 (tail = 36-42 µm); V = 68-70.
* 10 males: L = 0.54-0.62 mm; a = 36-39 (width = 14-17 µm); b = 8.6-8.8 (oesophagus = 63-66 µm); c = 15-17 (tail = 34-37 µm).
(After Allen, 1952):
* females: L = 0.62-0.88 mm; a = 38-58; b = 9-12; c = 15-20; V = 43-3366-724-8.
* males: L = 0.44-0.72 mm; a = 36-47; b = 9-11; c = 14-19; T = 50-65.
(From rice seeds from Séfa, Senegal; after Fortuner, 1970):
* 20 females: L = 0.57-0.84 (0.68) mm; a = 39-53 (47.7); b = 9.2-13.1 (11.46); b' = 4.06-5.77 (4.85); c = 13.8-20.4 (17.7); V = 39..1-19..968.7-73.6 (71.2)4.1-6.2; spear = 10.0-12.5 (11.9) µm.
* 9 males: L = 0.53-0.61 (0.57) mm; a = 40.7-46.9 (44.4); b = 8.87-10.70 (9.52); b' = 3.57-4.91 (4.09); c = 16-20 (17.97); T = 28-52 (40.59); spear = 10.0-12.5 (11.4) µm; spicules (dorsal limb) = 18-21 (19.2) µm.
Description (after Franklin & Siddiqi, 1972)
Female
The body of female A. besseyi is slender, straight to slightly arcuate ventrally when relaxed; annules fine, indistinct, about 0.9 µm wide near mid-body. Lip region rounded, unstriated, slightly offset and wider than body at lip base, about half as wide as mid-body; labial framework hexaradiate, lightly sclerotized. Lateral fields about one-fourth as wide as body, with 4 incisures. Anterior part of spear sharply pointed, about 45% of total spear length, posterior part with slight basal swellings which are 1.75 µm across. Median oesophageal bulb oval, with a distinct valvular apparatus slightly behind its centre. Oesophageal glands extending dorsally and subdorsally for 4 to 8 body-widths over intestine. Nerve ring about one body-width behind median oeosphageal bulb.
Excretory pore usually near anterior edge of nerve ring. Hemizonid 11-15 µm behind excretory pore. Vulva transverse, with slightly raised lips. Spermatheca elongate oval (up to 8 times as long as wide when fully distended), usually packed with sperm. Ovary relatively short and not extending to oesophageal glands, with oocytes in 2-4 rows. Post-vulva uterine sac narrow, inconspicuous, not containing sperm, 2.5-3.5 times anal body width long but less than one-third distance from vulva to anus. Tail conoid, 3.5-5 anal body widths long; terminus bearing a mucro of diverse shape with 3-4 pointed processes.
Male
Male A. besseyi are about as numerous as females. The posterior end of body is curved to about 180 degrees in relaxed specimens. Lip region, spear and oesophagus as described for female; tail conoid, with terminal mucro with 2-4 pointed processes. First pair of ventrosubmedian papillae adanal, second slightly behind middle of tail and third subterminal. Spicules typical of the genus except that the proximal end lacks a dorsal process (apex) and has only a moderately developed ventral one (rostrum). Testis single, oustretched.
Distribution
Top of pageA. besseyi is very widely distributed and now occurs in most rice growing areas (Ou, 1985). Its wide distribution has resulted from dissemination in seed.
See also CABI/EPPO (1998, No. 157).
Distribution Table
Top of pageThe distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
Last updated: 24 May 2022Continent/Country/Region | Distribution | Last Reported | Origin | First Reported | Invasive | Reference | Notes |
---|---|---|---|---|---|---|---|
Africa |
|||||||
Benin | Present | ||||||
Burkina Faso | Present | ||||||
Burundi | Present | ||||||
Cameroon | Present | ||||||
Central African Republic | Present | ||||||
Chad | Present | ||||||
Comoros | Present | ||||||
Congo, Democratic Republic of the | Present | ||||||
Côte d'Ivoire | Present | ||||||
Egypt | Present | ||||||
Gabon | Present | ||||||
Gambia | Present | ||||||
Ghana | Present | ||||||
Guinea | Present | ||||||
Kenya | Present, Widespread | ||||||
Madagascar | Present | ||||||
Malawi | Present | ||||||
Mali | Present | ||||||
Niger | Present | ||||||
Nigeria | Present | ||||||
Rwanda | Present | ||||||
Senegal | Present | ||||||
Sierra Leone | Present | ||||||
South Africa | Present, Localized | ||||||
Tanzania | Present, Widespread | ||||||
Togo | Present | ||||||
Uganda | Present | ||||||
Zambia | Present | ||||||
Zimbabwe | Present | ||||||
Asia |
|||||||
Afghanistan | Present | ||||||
Azerbaijan | Present | ||||||
Bangladesh | Present, Widespread | ||||||
Cambodia | Present | ||||||
China | Present | Introduced | 1889 | ||||
-Anhui | Present | ||||||
-Fujian | Present | ||||||
-Guangdong | Present | ||||||
-Guangxi | Present | ||||||
-Guizhou | Present | ||||||
-Hebei | Present | ||||||
-Henan | Present | ||||||
-Hubei | Present | ||||||
-Hunan | Present | ||||||
-Jiangsu | Present | ||||||
-Jiangxi | Present | ||||||
-Jilin | Present | ||||||
-Liaoning | Present | ||||||
-Ningxia | Present | ||||||
-Shaanxi | Present | ||||||
-Shandong | Present | ||||||
-Shanxi | Present | ||||||
-Sichuan | Present | ||||||
-Xinjiang | Present | ||||||
-Zhejiang | Present | ||||||
Georgia | Present, Widespread | ||||||
India | Present, Widespread | ||||||
-Andaman and Nicobar Islands | Present | ||||||
-Andhra Pradesh | Present | ||||||
-Assam | Present, Widespread | ||||||
-Bihar | Present, Widespread | ||||||
-Delhi | Present, Widespread | ||||||
-Gujarat | Present | ||||||
-Haryana | Present, Widespread | ||||||
-Jammu and Kashmir | Present | ||||||
-Jharkhand | Present | ||||||
-Karnataka | Present | Original citation: Ramakrishnan and Rajendran (2003) | |||||
-Kerala | Present | ||||||
-Madhya Pradesh | Present, Widespread | ||||||
-Maharashtra | Present, Widespread | ||||||
-Meghalaya | Present | ||||||
-Odisha | Present | ||||||
-Punjab | Present | ||||||
-Tamil Nadu | Present | ||||||
-Tripura | Present, Widespread | ||||||
-Uttar Pradesh | Present, Widespread | ||||||
-West Bengal | Present | ||||||
Indonesia | Present | ||||||
Iran | Present | ||||||
Israel | Absent, Formerly present | ||||||
Japan | Present | ||||||
-Honshu | Present | ||||||
-Kyushu | Present | ||||||
-Shikoku | Present | ||||||
Kyrgyzstan | Present | ||||||
Laos | Present | ||||||
Malaysia | Present | ||||||
-Peninsular Malaysia | Present | ||||||
Myanmar | Present | ||||||
Nepal | Present, Localized | ||||||
North Korea | Present | ||||||
Pakistan | Present | ||||||
Philippines | Present | ||||||
Singapore | Present, Few occurrences | ||||||
South Korea | Present | ||||||
Sri Lanka | Present | ||||||
Taiwan | Present, Widespread | ||||||
Tajikistan | Present, Localized | ||||||
Thailand | Present | ||||||
Turkey | Present, Localized | ||||||
Uzbekistan | Present | ||||||
Vietnam | Present | ||||||
Europe |
|||||||
Belgium | Absent | ||||||
Bulgaria | Present, Localized | First reported: 197* | |||||
France | Absent, Formerly present | ||||||
Hungary | Present, Localized | 1970 | |||||
Italy | Present, Localized | 1973 | |||||
Netherlands | Present, Transient under surveillance | Oryza: absent, no pest records; Fragaria: absent, confirmed by survey; few ornamental greenhouse crops (not related to Fragaria and Oryza): transient, actionable, under surveillance. Based on long-term annual surveys, 10 survey observations in 2012. | |||||
Portugal | Absent, Confirmed absent by survey | ||||||
Romania | Present, Localized | ||||||
Russia | Present, Localized | ||||||
-Southern Russia | Present | ||||||
Slovakia | Absent, Invalid presence record(s) | ||||||
Slovenia | Absent | ||||||
Ukraine | Present, Localized | ||||||
United Kingdom | Absent, Intercepted only | ||||||
North America |
|||||||
Cuba | Present | ||||||
Dominica | Present | ||||||
Dominican Republic | Present | ||||||
El Salvador | Present | ||||||
Guadeloupe | Present | ||||||
Mexico | Present | ||||||
Panama | Present | ||||||
Trinidad and Tobago | Absent, Intercepted only | ||||||
United States | Present, Localized | ||||||
-Arkansas | Present | ||||||
-California | Present | ||||||
-Florida | Present | ||||||
-Hawaii | Present | ||||||
-Louisiana | Present | ||||||
-Texas | Present | ||||||
Oceania |
|||||||
Australia | Present, Localized | ||||||
-Northern Territory | Present | ||||||
-Queensland | Present | ||||||
Cook Islands | Present | ||||||
Fiji | Present | ||||||
Papua New Guinea | Present | ||||||
South America |
|||||||
Argentina | Absent, Invalid presence record(s) | ||||||
Brazil | Present | ||||||
-Alagoas | Present | ||||||
-Bahia | Present | ||||||
-Mato Grosso | Present | ||||||
-Minas Gerais | Present | ||||||
-Parana | Present, Localized | ||||||
-Rio Grande do Norte | Present | ||||||
-Rio Grande do Sul | Present | ||||||
-Santa Catarina | Present | ||||||
-Sao Paulo | Present | ||||||
-Sergipe | Present | ||||||
Ecuador | Present, Few occurrences |
Risk of Introduction
Top of pageECONOMIC IMPORTANCE High
DISTRIBUTION Worldwide
SEEDBORNE INCIDENCE High
SEED TRANSMITTED Yes
SEED TREATMENT Yes
OVERALL RISK High
Notes on phytosanitary risk
A. besseyi already has a world wide distribution but should remain a quarantine pest in rice growing countries because of the potential danger of the emergence of more virulent pathotypes. Seeds for export should be treated with hot water, unless nematode-free seed can be ensured.
Habitat
Top of pageHost Plants and Other Plants Affected
Top of pageSymptoms
Top of pagePlants susceptible to A. besseyi can be symptomless but yield loss only occurs in plants showing some symptoms. During early growth, the most conspicuous symptom is the emergence of the chlorotic tips of new leaves from the leaf sheath. These tips later dry and curl, whilst the rest of the leaf may appear normal. The young leaves of infected tillers can be speckled with a white splash pattern or have distinct chlorotic areas. Leaf margins may be distorted and wrinkled but leaf sheaths are symptomless.
The viability of A. besseyi infected seed is lowered and germination is delayed (Tamura and Kegasawa, 1959b) and diseased plants have reduced vigour and height (Todd and Atkins, 1958). Infected panicles are shorter, with fewer spikelets and a smaller proportion of filled grain (Dastur, 1936; Yoshii, 1951; Todd and Atkins, 1958).
In severe infections, the shortened flagleaf is twisted and can prevent the complete extrusion of the panicle from the boot (Yoshii and Yamamoto, 1950a; Todd and Atkins, 1958). The grain is small and distorted (Todd and Atkins, 1958) and the kernel may be discoloured and cracked (Uebayashi et al., 1976). Infected plants mature late and have sterile panicles borne on tillers produced from high nodes.
Strawberry
A. besseyi is a foliar pest of strawberry and may be found between leaves and buds. Aphelenchoides spp. cause distortion of the leaves which is more noticeable on newly formed leaves after growth resumes in spring in areas of the USA, south of Virginia and Arkansas, and also in Australia (Brown et al., 1993).
List of Symptoms/Signs
Top of pageSign | Life Stages | Type |
---|---|---|
Inflorescence / discoloration panicle | ||
Inflorescence / twisting and distortion | ||
Leaves / abnormal colours | ||
Leaves / abnormal forms | ||
Leaves / abnormal patterns | ||
Seeds / discolorations | ||
Seeds / empty grains | ||
Seeds / lesions on seeds | ||
Stems / stunting or rosetting | ||
Whole plant / dwarfing |
Biology and Ecology
Top of pageRice
After sowing, anabiotic A. besseyi rapidly become active and are attracted to meristematic areas. During early growth, it is found in low numbers within the innermost leaf sheath, feeding ectoparasitically around the apical meristem (Yoshii and Yamamoto, 1950b; Goto and Fukatsu, 1952; Todd and Atkins, 1958). The main stem is frequently more infected than subsequent tillers (Goto and Fukatsu, 1952). A rapid increase in nematode numbers takes place at later tillering (Goto and Fukatsu, 1952) and is associated with the reproductive phase of plant growth (Huang and Huang, 1972).
Nematodes are able to enter spikelets before anthesis, within the boot, and feed ectoparasitically on the ovary, stamens, lodicules and embryo (Dastur, 1936; Huang and Huang, 1972). However, A. besseyi is more abundant on the outer surface of the glumes and enters when these separate at anthesis (Yoshii and Yamamoto, 1950b). As grain filling and maturation proceed, reproduction of the nematode ceases, although the development of J3 to adult continues until the hard dough stage (Huang and Huang, 1972). The population of anabiotic nematodes is predominantly adult females (Huang et al., 1979). These nematodes coil and aggregate in the glume axis. More nematodes occur in filled grain than in sterile spikelets (Yoshii and Yamamoto, 1950b) and infected grain tends to occur more towards the middle of the panicle (Goto and Fukatsu, 1952).
A. besseyi is amphimictic (Huang et al., 1979) and males are usually abundant, however, reproduction can be parthenogenetic. The optimum temperature for oviposition and hatching is 30°C. At 30°C the life cycle is 10±2 days and lengthens significantly at temperatures <20°C (Huang et al., 1972). No development occurs below 13°C (Sudakova, 1968).
A. besseyi aggregate in the glume axis of maturing grain and slowly desiccate as kernel moisture is lost. They become anabiotic and are able to survive for 8 months to 3 years after harvest (Cralley, 1949; Yoshii and Yamamoto, 1950b; Todd, 1952; Todd and Atkins, 1958). Survival is enhanced by aggregation and a slow rate of drying (Huang and Huang, 1974), but the number (Yoshii and Yamamoto, 1950b; Sivakumar, 1987a) and infectivity (Cralley and French, 1952) of nematodes is reduced as seed age increases. It is ironic that good seed storage conditions probably prolong nematode survival.
A. besseyi is not thought to survive long periods in soil between crops (Cralley and French, 1952; Yamada et al., 1953) although anabiotic nematodes may survive on rice husks and plant debris. Sivakumar (1987b) found A. besseyi reproducing on Curvularia and Fusarium in straw after harvest.
The principal dispersal method for A. besseyi is seed. It can be transmitted in flood water in lowland rice (Tamura and Kegasawa, 1958) but the survival of nematodes in water decreases as temperature increases from 20 to 30°C (Tamura and Kegasawa, 1958). High seeding rates in infected seed beds facilitates local dispersal (Kobayashi and Sugiyama, 1977).
Strawberry
A. besseyi is a foliar pest of strawberry and may be found between leaves in buds. The nematode has rapid life cycles (2-3 weeks) and thrive in moist conditions which enable them to move over plant surfaces in water films (Brown et al., 1993).
Natural enemies
Top of pageNatural enemy | Type | Life stages | Specificity | References | Biological control in | Biological control on |
---|---|---|---|---|---|---|
Arachnula impatiens | Pathogen | |||||
Vampyrella vorax | Pathogen |
Seedborne Aspects
Top of pageIncidence
Surveys have shown large numbers of seed lots to be infected with, and high incidences of infection by, A. besseyi throughout the main rice producing areas of the world. In Tanzania, A. besseyi was reported in 12.8% of rice seed lots with infection levels ranging from 2 to 82% within lots (Taylor et al., 1972). About 70% of the samples of rice grains from 32 plantations in central west Brazil were infected. The numbers of nematodes ranged from 10 to >140 nematodes/100 grains (Huang et al., 1977). A. besseyi was recovered from 5.5% of 474 seed samples obtained from rice seed warehouses in Louisiana, USA (McGawley et al., 1984). In Malaysia, 80% of seed lots from four major rice growing areas showed the presence of A. besseyi (Rahmin, 1988). A. besseyi has also been found in the seeds of Stylosanthes hamata (Gokte et al, 1992), Fraxinus americana (Gokte et al., 1989) and Panicum maximum (Merny et al., 1985).
The process of infection of the seeds begins after sowing, when anabiotic A. besseyi rapidly become active and are attracted to meristematic areas of the developing seedling (Nandakumar et al., 1975). During early growth, it is found in low numbers within the innermost leaf sheath, feeding ectoparasitically around the apical meristem (Yoshii and Yamamoto, 1950b; Goto and Fukatsu, 1952; Todd and Atkins, 1958). The main stem is frequently more infected than subsequent tillers (Goto and Fukatsu, 1952). A rapid increase in nematode numbers takes place at later tillering (Goto and Fukatsu, 1952) and is associated with the reproductive phase of plant growth (Huang and Huang, 1972).
Nematodes are able to enter spikelets before anthesis, within the boot, and feed ectoparasitically on the ovary, stamens, lodicules and embryo (Dastur, 1936; Huang and Huang, 1972). However, A. besseyi is more abundant on the outer surface of the glumes and enters when these separate at anthesis (Yoshii and Yamamoto, 1950b). As grain filling and maturation proceed, reproduction of the nematode ceases, although the development of J3 to adult continues until the hard dough stage (Huang and Huang, 1972). The population of anabiotic nematodes is predominantly adult females (Huang et al., 1979). These nematodes coil and aggregate in the glume axis. More nematodes occur in filled grain than in sterile spikelets (Yoshii and Yamamoto, 1950b) and infected grain tends to occur more towards the middle of the panicle (Goto and Fukatsu, 1952).
A. besseyi aggregate in the glume axis of maturing grain and slowly desiccate as kernel moisture is lost. They become anabiotic and are able to survive for 8 months to 3 years after harvest (Cralley, 1949; Yoshii and Yamamoto, 1950b; Todd, 1952; Todd and Atkins, 1958). Survival is enhanced by aggregation and a slow rate of drying (Huang and Huang, 1974), but the number (Yoshii and Yamamoto, 1950b; Sivakumar, 1987a) and infectivity (Cralley and French, 1952) of nematodes is reduced as seed age increases. It is ironic that good seed storage conditions probably prolong nematode survival.
Togashi and Hoshino (2001) investigated relationships between the number of A. besseyi per seed, size of seed harbouring nematodes, and nematode mortality on 18 panicles collected from 12 paddy fields (in Japan) showing three different levels of white tip disease. The panicles were investigated after storage for 30-82 days at 4°C. There was no nematode mortality within seeds during storage. Mean nematode number per seed increased and mean degree of seed swelling decreased as the paddy field infestation of white tip disease increased. For paddy field means, there was a significant negative correlation between the mean nematode number per seed and the mean degree of rice seed swelling. Intriguingly, for individual seeds, the mean degree of swelling increased up to that typical of well-developed seeds with increasing nematode number per seed. Nematode mortality occurred in an inversely density-dependent fashion within individual seeds. The nematode exhibited a clumped distribution among seeds in each paddy field. Such ecological features of the nematode might contribute to its persistence in rice plant populations.
Effect on Seed Quality
Seeds infected with A. besseyi are capable of germination, but hot water treatment to control the nematode reduced germination of some varieties (Rahim, 1988). According to Tsay et al. (1998), 16% of A. besseyi survived under desiccation at 70°C for 12 h, and the germination of rice seed decreased to 44%. At 60°C, 40% of A. besseyi survived and there was no effect on rice seed germination.
Pathogen Transmission
Seed
The principal dispersal method for A. besseyi is seed. Nandakumar et al. (1975) showed that the nematodes were activated from their dormant state by soaking infested rice seeds in water at 28°C for 12 to 15 hours. They then feed on the tender primordium of the sprouting seeds but later migrate to the leaf as it unfurls. Symptoms of white-tip disease appear on leaves 16 days after germination. A. besseyi adapts to seed transmission through its capacity to remain quiescent upon dehydration and reactivate with rehydration. In northern Italy, where conditions were unfavorable for the overwinter survival of A. besseyi, phytosanitary measures such as the exclusion of infested seeds were effective in reducing the spread of the nematode in paddy crops (Bergamo et al., 2000).
The number of studies undertaken on crop losses due to the nematode is very limited, but an inverse correlation between the number of nematodes in seeds and crop performance has been convincingly demonstrated (Huang, 1983). Generally, population densities per seed number or weight are counted. Fukano (1962) determined an economic damage threshold density (300 live nematodes/100 seed). It has been shown that high seeding rates in infected seed beds facilitates local dispersal of the pathogen (Kobayashi and Sugiyama, 1977).
Other sources
A. besseyi can be transmitted in flood water in lowland rice (Tamura and Kegasawa, 1958) but the survival of nematodes in water decreases as temperature increases from 20 to 30°C (Tamura and Kegasawa, 1958). The nematode also lives in rice stubble left in the field after harvest which enables transfer of the inoculum from season to season (Sivakumar, 1987).
Seed Treatment
There are numerous variations of methods for the hot-water treatment of rice seed (Cralley, 1949, 1952; Yoshii and Yamamoto, 1950c, 1951; Todd and Atkins, 1958; Borokova, 1967). The most effective control of A. besseyi requires seed to be pre-soaked in cold water for 18-24 hours and immersed in water at 51-53°C for 15 minutes. Higher temperatures (55-61°C for 10-15 minutes) are required if seed is not pre-soaked. The temperature and duration of treatment must be closely monitored and, after treatment, the seed must be dried at 30-35°C, or sun-dried if stored, but otherwise can be sown directly in the field. Garcia et al. (2000) eradicated A. bessseyi by heat treatments, wet (60°C/10 minutes and 57°C/15 minutes) and dry (90°C/6 and 12 h and 95°C/6 and 12 h). Hoshino and Togashi (2000) showed that nematicides alone caused little nematode mortality within seeds. Most mortality occurred while seeds were being air-dried. Mortality caused by air-drying alone was 1.7 times greater than that caused by soaking seeds in water for 24 hours.
For quarantine purposes at the International Rice Research Institute (IRRI), seed is soaked in cold water for 3 hours followed by hot water at 55°C for 15 minutes. Tenente and Manso (1994) studied rice seeds infested with A. besseyi either immersed in water at 52, 54 and 57°C for 10 and 15 minutes, with and without shaking, or treated with water solutions at 32 and 33 ml/100 ml of thiabendazole (40%). Thiabendazole decreased the nematode population. Heat treatment with shaking at all temperatures and the 57°C/10 minute treatment without shaking also allowed eradication. Only the heat treatment at 52°C for 15 minutes with shaking gave eradication of A. besseyi without affecting germination, and is thus considered as the most appropriate control method. Giudici et al. (2004) found that seed immersion for 10-15 minutes in water at 55-61°C eradicated seedborne A. besseyi without reducing germination.
Various chemical seed treatments have been used for the control of A. besseyi including demeton, malathion and fensulfothion. Lee et al. (1972) reported effective control by treating water or by root dipping with diazinon and nemagon. A. besseyi control with carbosulfore sprays has been reported (Rao et al., 1986), but pre-harvest chemical treatment alone is only partially effective (Aleksandrova, 1981). The timing of application is important.
Ultrasound and gamma irradiation have also been investigated for their potential in eradicating A. besseyi from seeds (Aleksandrova 1985; Nagy, 1987).
Seed treatment with dipotassium hydrogen phosphate, coupled with a foliar spray of salicylic acid effectively managed A. besseyi in the field in Karnataka, India, and increased the yield by 3.59% (Ramakrishnam and Raiendran, 2003a). Seed treatment with Pseudomonas flourescens, followed by foliar applications of P. flourescens at 45, 55 and 65 days after sowing, reduced chaffiness in rice (caused by A. besseyi) by 56.5% (Ramakrishnam and Raiendran, 2003b). Mohanty et al. (2004) recommend soaking rice seeds in 0.075% cartap hydrochloride for 12 hours, which resulted in 82.02% mortality of seedborne A. besseyi and a significant increase in grain yield.
Biocontrols were trailed in Ghana by Osei and Sackey-Asante (2006). Seed dressing treatment with ground pepper (Capsicum frutescens cv. Legon 18), ground neem seeds (Azadirachta indica) and wood ash, all at 15 g/kg, reduced seedborne populations of A. besseyi by 83.5%, 82.4% and 71.7%, respectively. However, the treatments also inhibited seed germination by 9.6-24.4%, with ground pepper resulting in the greatest reduction.
Seed Health Tests
Manual dehulling (Huang, 1983; Prot and Gergon, 1994)
- Soak seeds in water for 24 hours.
- Dehull seeds with a scalpel and needle.
- Transfer contents (kernels, hulls and water) to a Baermann funnel or a sieve.
- Recover and count nematodes after 48-72 hours.
Modified Baermann or Seive method (Gergon and Mew, 1991; Prot and Gergon, 1994)
- Place seeds over a 10 cm, 40 x 40 mesh steel wire dish in a funnel (12 cm in diameter) and filled with 250 ml water.
- Let it stand for at least 48 hours.
- After incubation, draw ca 20 ml of water into a test tube through a rubber tube attached to the bottom of the funnel.
- Allow the collected water to stand for 1 hour.
- Pipette out excess water and leave 10-15 ml in the test tube.
- Examine the remaining water for nematodes.
Notes on Methods
A mass extraction method has been described (Hoshino and Togashi, 2002). Common methods of nematode extraction applied to Panicum maximum seeds infested with A. besseyi have been compared by Bueno et al. (2002).
Pathway Vectors
Top of pageVector | Notes | Long Distance | Local | References |
---|---|---|---|---|
Containers and packaging - wood | Yes | |||
Land vehicles | Yes | |||
Rice seeds | Yes | |||
Plants or parts of plants | Grasses in paddy fields | Yes | ||
Soil, sand and gravel | Yes |
Plant Trade
Top of pagePlant parts liable to carry the pest in trade/transport | Pest stages | Borne internally | Borne externally | Visibility of pest or symptoms |
---|---|---|---|---|
Bulbs/Tubers/Corms/Rhizomes | nematodes/adults; nematodes/eggs; nematodes/juveniles | Yes | Yes | Pest or symptoms not visible to the naked eye but usually visible under light microscope |
Flowers/Inflorescences/Cones/Calyx | nematodes/adults; nematodes/eggs; nematodes/juveniles | Yes | Yes | Pest or symptoms not visible to the naked eye but usually visible under light microscope |
Leaves | nematodes/adults; nematodes/eggs; nematodes/juveniles | Yes | Yes | Pest or symptoms not visible to the naked eye but usually visible under light microscope |
Stems (above ground)/Shoots/Trunks/Branches | nematodes/adults; nematodes/eggs; nematodes/juveniles | Yes | Yes | Pest or symptoms not visible to the naked eye but usually visible under light microscope |
True seeds (inc. grain) | nematodes/adults; nematodes/eggs; nematodes/juveniles | Yes | Yes | Pest or symptoms not visible to the naked eye but usually visible under light microscope |
Plant parts not known to carry the pest in trade/transport |
---|
Bark |
Fruits (inc. pods) |
Growing medium accompanying plants |
Roots |
Seedlings/Micropropagated plants |
Wood |
Impact
Top of pageRice
A. besseyi is widely distributed because of its dissemination in seed, but its importance varies between regions, countries and localities. Within a locality, the incidence and severity of the disease can change from year to year, and is strongly influenced by cultural practices and local rice types. Infection and damage are generally greater in lowland and deep water systems than in upland environments. However, losses of up to 50% have been reported in upland rice in Brazil (da Silva, 1992).
Damage in a susceptible cultivar largely depends on the percentage of infested seed sown and the number of A. besseyi/infested seed. With few exceptions, the former has rarely been determined despite its importance in governing the number of infection loci in a field. Generally, population densities/seed number or weight are counted. Fukano (1962) determined an economic damage threshold density (300 live nematodes/100 seed).
In the 1950s typical figures for susceptible cultivars in the USA were 17.5, 4.9 and 6.6% in different years (Atkins and Todd, 1959) and 10-30% in Japan (Yamada and Shiomi, 1950; Yoshii and Yamamoto, 1950a; Yoshii, 1951). Tsay et al. (1998) reported yield losses of 44.9, 34.7 and 24.2% when rice plant infestation rates were 57, 34 and 18%, respectively. A. besseyi has been controlled in the USA by seed treatment and the use of resistant cultivars and is no longer a pest (Hollis and Keoboonrueng, 1984). A. besseyi also disappeared from Japan but has re-occurred, the economic value of infected discoloured grain being reduced if infection exceeds 0.7% (Inagaki, 1985).
A. besseyi damage has been reported from deep water rice in Bangladesh. More than 50% of fields were infected and the panicle weight of heavily infected plants (650 nematodes/100 seed) was a third that of less infected plants (112 nematodes/100 seed) (Rahman and McGeachie, 1982; Rahman and Taylor, 1983). In contrast, local cultivars in Thailand appear to be tolerant of A. besseyi and no symptoms have been observed despite widespread infection (Buangsuwon et al., 1971).
Economic loss in the Philippines has not been reported, but infection varies according to year, season and cultivar (Madamba et al., 1974). Levels of infested seed are generally low (4.7-7% over 5 years) (Madamba et al., 1981), and severe damage is unlikely as high numbers of A. besseyi (210-5300/100 seed) are not always associated with a high percentage of infested seed.
A. besseyi is thought to be an important pest in India. Rao (1976) reported severe symptoms in the field, but accurate yield loss assessment is lacking. Muthukrishnan et al. (1974) observed that plants sometimes recover after early severe damage and computed losses of 0.2-10%. Infestation levels in Sri Lanka are not considered important (Lamberti and Robini, 1980).
Strawberry
A. besseyi is an important pest of strawberry in the USA, south of Arkansas and Virginia (Brown et al., 1993).
Diagnosis
Top of pageA diagnostic protocol for A. besseyi is given in OEPP (2004). The diagnosis of A. besseyi from abnormal rice grains in China is detailed in Lin et al. (2005).
A. Besseyi was identified in forage grasses in Brazil by observing morphological features under the light and scanning electron microscopes in Favoreto et al. (2011).
Detection and Inspection
Top of pageSimilarities to Other Species/Conditions
Top of pagePrevention and Control
Top of pageDue 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.
Preventing the dispersal of A. besseyi in rice requires the elimination of nematodes from seed; hot water or chemical seed treatments are commonly used. Resistant cultivars and cultural methods have been used to reduce infection below damage thresholds, and tolerant cultivars avoid yield loss without nematode control. Stubble burning prevents transmission of A. besseyi in straw and chaff but would have to be used in conjunction with other control measures.
Hot water treatment
There are numerous variations of methods for the hot water treatment of rice seed (Cralley, 1949, 1952; Yoshii and Yamamoto, 1950c, 1951; Todd and Atkins, 1958; Borokova, 1967). The most effective control requires seed to be pre-soaked in cold water for 18-24 hours, then immersed in water at 51-53°C for 15 minutes. Higher temperatures (55-61°C for 10-15 min) are required if seed is not pre-soaked. The temperature and duration of treatment must be closely monitored and, after treatment, the seed must be dried at 30-35°C, or sun dried if stored, but otherwise can be sown directly in the field. For quarantine purposes at the International Rice Research Institute, seed is soaked in cold water for 3 hours followed by hot water at 55°C for 15 minutes.
Chemical Control
Various chemical seed treatments have been used for the control of A. besseyi including demeton, malathion and fensulfothion. Lee et al. (1972) reported effective control by treating water or by root dipping with diazinon and nemagon. A. besseyi control with carbosulfore sprays has been reported (Rao et al., 1986), but pre-harvest chemical treatment alone is only partially effective (Aleksandrova, 1981). The timing of application is important.
Host-Plant Resistance
Resistance to A. besseyi is widespread. In the USA, A. besseyi has been controlled principally through the use of resistant cultivars. Resistance to A. besseyi has subsequently been reported from Japan (Nishizawa, 1953b); Yamada et al., 1953; Goto and Fukatsu, 1956), Korea (Park and Lee, 1976), India (Rao et al., 1986), Brazil (Oliveira and Ribeiro, 1980; da Silveira et al., 1982), USSR (Popova et al., 1980) and Italy (Orsenigo, 1954). Resistance to A. besseyi is thought to be genetically controlled and carried by the Japanese cultivar Asi-Hi (Nishizawa, 1953).
Symptomless but susceptible (i.e. tolerant) cultivars (Nishizawa, 1953; Goto and Fukatsu, 1956) are common. Symptom expression in the field is particularly variable (Atkins and Todd, 1959) and variations between plants of a cultivar also occur (Orsenigo, 1954). In Thailand, all local cultivars are considered tolerant of A. besseyi (Buangsuwon et al., 1971).
Cultural Control
Irrigating seed beds (Yamada et al., 1953) or direct seeding into water (Cralley, 1956) reduces infection by A. besseyi. In these conditions, nematodes emerge and lose vigour before seed germination. High seedling rates in the seed bed (Kobayashi and Sugiyama, 1977) and high numbers of seedlings/hill (Yamada et al., 1953) tend to increase infection by increasing the number of infection loci in the field. Such problems are thought to be responsible for the re-occurrence of A. besseyi in Japan (Inagaki, 1985). In the USA (Cralley, 1949) and Japan (Yoshi and Yamamoto, 1951; Yamada et al., 1953), early planting, presumably in cooler conditions, reduced or eliminated A. besseyi infection.
Summary of Control Measures
- Hot water treatment of seed. Probably the most effective and cheapest control measure
- Resistant or tolerant cultivars
- Early planting if rice season is preceded by a cooler period
- Low seed bed planting densities
In strawberry, control is possible by hot water treatment of planting stocks, or regeneration of plants from dormant excised axillary buds. Host weed control and planting healthy runners in clean soil is the basis for ensuring freedom from problems.
References
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Allen MW, 1952. Taxonomic status of the bud and leaf nematodes related to Alphelenchoides fragariae (Ritzema Bos, 1891). Proc. Helminth. Soc. Wash., 19(2):108-120
Ancalmo O, Davis WC, 1962. Diseases of rice in new El Salvador. Plant Disease Reporter, 46(4):293
Anon., 1971. Queensland Department of Primary Industries. Annual Report 1970-71. Brisbane, Australia: Queensland Department of Primary Industries, 56 pp.
Anon., 1972. Iconographia Cormophytorum Sinicorum, Tomus 1.
APPPC, 1987. Insect pests of economic significance affecting major crops of the countries in Asia and the Pacific region. Technical Document No. 135. Bangkok, Thailand: Regional Office for Asia and the Pacific region (RAPA)
Atkins JG, Todd EH, 1959. White tip disease of rice. III. Yield tests and varietal resistance. Phytopathology, 49:189-191
AVA, 2001. Diagnostic records of the Plant Health Diagnostic Services, Plant Health Centre, Agri-food & Veterinary Authority, Singapore
Barat H, Delassus M, Vuong Huu Hai, 1966. Présence en Casamance de l'anguillule de feuilles de riz, Aphelenchoides besseyi Christie 1942. Agron. Trop, Nogent, 21(1):47-55. [English & Spanish summaries, p. 55]
Barat H, Delassus M, Vuong Huu, Hai, 1969. The geographical distribution of white tip nematode disease of rice in tropical Africa and Madagascar. In: Peachey JE, ed. Nematodes of tropical crops. Technical Comunication Commonwealth Bureau of Helminthology, No. 40: 269-273
Borovkora AM, 1972. White tip disease of rice in the USSR and its control. In: Sveshnikova NM, ed. Nematode Diseases of Agricultural Plants. Proceedings of the All-Union Conference on Plant Nematology, 131-134
Borovkova AM, 1967. Aphelenchoides besseyi in the USSR and its control.] In: Sveshnikova NM, ed. [Nematode diseases of crops. Moscow: Izdatekstvo 'Kolos', 153-157
Bueno ERV, Prates M, Tenente RCV, 2002. Evaluation of common methods of nematode extraction applied to Panicum maximum seeds infested with Aphelenchoides besseyi. Nematologia Brasileira, 26(2):213-217
Christie JR, 1942. Proc. Helminth. Soc. Wash., 9:82-84
Cralley EM, 1949. White tip of rice. Phytopathology, 39:5
Cralley EM, 1952. Control of white tip of rice. Arkansas Farm Research, 1:6
Cralley EM, 1956. A new control measure for white tip. Arkansas Farm Research, 5:5
Cralley EM, Adair CR, 1949. Rice diseases in Arkansas in 1948. Plant Disease Reporter, 33:257-259
Cralley EM, French RG, 1952. Studies on the control of white tip of rice. Phytopathology, 42:6
Dastur JF, 1936. A nematode disease of rice in the Central Provinces. Proceedings of the Indian Academy of Sciences, Section B, 4:108-121
EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm
EPPO, 2018. EPPO Global Database (available online). https://gd.eppo.int
Fernandez Diaz Siveira M, 1967. Lista de nematodes de Cuba. Revta Agric., Habana, 1:74-88
Fortuner R, 1970. On the morphology of Aphelenchoides besseyi Christie, 1942 and A Siddiqii n.sp. (Nematoda, Aphelenchoidea). J. Helminth., 44(2):141-152
Franklin MT, Siddiqi MR, 1972. Aphelenchoides besseyi. CIH Descriptions of Plant Parasitic Nematodes, Set 1, No. 4
Fukano H, 1962. Control method against rice white tip disease. Nogyo oyobi Engei, 37:689-692
Goto K, Fukatsu R, 1952. Studies on white tip of rice plant caused by Aphelenchoides oryzae Yokoo. II. Number and distribution of the nematode on the affected plants. Annals of the Phytopathological Society of Japan, 16:57-60
Goto K, Fukatsu R, 1956. Studies on the white tip of rice plant. III. Analysis of varietal resistance and its nature. Bulletin of the National Institue of Agricultural Sciences, Tokyo. Series C. Plant Pathology and Entomology, (6):123-149
Hashoika Y, 1964. Nematode diseases of rice in the world. Riso, 13(2):139-147
Hooper DJ, Merny G, 1966. Outbreaks and new records: Sierra Leone and Senegal. Two rice nematodes new for Africa". Plant Protection Bulletin FAO, 14(1):25-26
Inagaki H, 1985. The plant parasitic nematodes important in Japan and the related researches. JARQ, 18:194-201
Javor I, 1970. A rizsfonálféreg (Aphelenchoides besseyi Christie) hazai felderftésének tapasztalatai. Novényvédelem, 6:259-263
Kermarrec A, Anais A, 1973. Presencia en Guadeloupe de Aphelenchoides besseyi Christie 1942 (Nematoda, Aphelenchoidae) en follaje del mapney: Dioscorea trifida L. Comm. V1 Congr. ONTA, Maracay, Venezuela, 1-6 Oct. 1973, 11 pp
Lamberti F, Rodini KE, 1980. Importance of plant parasitic nematodes in Sri Lanka and recommendations for control measures and future work. Proceedings of the Second Asian Symposium on Plant Diseases in the Tropics. Bangkok, Thailand, 144
Lordello LGE, 1969. OcorOncia du nematoide Aphelenchoides besseyi em arroz no Brasil. Revta Agric., S. Paolo, 44(4):129-131
Madamba CP, Sukit V, Adamo JA, 1974. Incidence of plant parasitic nematodes associated with rice grown in the Philippines. In: Proceedings of the International Rice Research Conference, 1974. Los Ba±os, Philippines: International Rice Research Institute, 4
Merny G, 1970. Les nématodes phytoparasites de riziFres inondées de la Côte d'Ivoire. I. Les espFces observées. Cahiers de l'ORSTOM, Sér. Biol. No. 11: 3-43
Merny G, Billard G, Pelletier R, 1985. Technique for eradication of Aphelenchoides besseyi (Nematoda: Aphelenchina) from seeds of Panicum maximum. Revue de Nematologie, 8(2): 155-160
Nishizawa T, 1953. Studies on the varietal resistance of rice plants to the rice nematode disease "Senchu shingar byo" (VI). Bulletin of the Kyushu Agricultural Experimental Station, 1:339-349
Orsenigo M, 1954. Suscettibilita di varieta Italiane di riso alla malattia della 'white-tip'. Annali della Facolta di Agraria Universita Cattolica del S. Cuore, Milano, 51:1-7
Ou SH, 1985. Rice diseases. Wallingford, UK; CAB International, 380 pp
Peachey JE, Larbey DW, Cain SC, 1966. White tip disease of rice in Africa. Helminth Abstr. 35(4):337-339
Preciado Castillo A, 1953. La enfermedad del arroz llamada punta blanca o white tip of rice. Campo Tucuba Ser 2, 20 (736), 82, 84, 86
Prot JC, Gergon EB, 1994. Nematodes. In: Mew TW, Misra JK, editors. A manual of rice seed health testing. Manila, Philippines; International Rice Research Institute, 47-48
Rahim MAA, 1988. Nematodes associated with paddy seeds in Malaysia Planti-Proceedings 1988, No. 3, 187-199. In: Proceedings of the symposium, Movement of pests and control strategies. Kuala Lumpar, Malaysia, 16-17 December, 1987
Rahman ML, Taylor B, 1983. Nematode pests associated with deepwater rice in Bangladesh. International Rice Research Newsletter, 8(5):20-21
Rao YS, Prasad JS, Panwar MS, 1986. Nematode problems in rice: crop losses, symptomatology and management. In: Swarup G, Dasgupta DR, eds. Plant Parasitic Nematodes of India: Problems and Progress. New Delhi, India: Indian Agricultural Research Institute, 279-299
Schotman CYL, 1989. Plant pests of quarantine importance to the Caribbean. RLAC-PROVEG, No. 21:80 pp
Siddiqi MA, 1970. White tip and ufra disease of rice. Plant Pathology Advisory Circular, Ministry of Agriculture and Natural Resources, Malawi, 4 pp
Silva GS da, 1992. White tip and national rice production. Informe Agropecuario Belo Horizonte 16:172, 57-59
Silveira SGP da, Curi SM, Fernandes CD, Bona A de, 1977. Occurrencia do nematoide Aphelenchoides besseyi Christie, 1942, em areas produtoras de sementes de arroz, no estado de Sao Paulo. Reunias de Nematologia, 2:81-91
Silveira SGP da, Curi SM, Souza DMde, Arruda HV de, 1982. Comportamento de algumas cultivares de arroz em relacao ao nematoide Aphelenchoides besseyi Christie, 1943. Biologico, 48:213-216
Stoyanov D, 1979. The nematode fauna of rice in Bulgaria. Rasteniev dni-Nauki, 16(1):115-120
Sudakova IM, Mastennikova VF, Dergunov ID, 1964. Effect of nitrate fertilisers on Aphelenchoides besseyi responsible for 'white tip' disease of rice. Zool. Zh., 43(11):1708-1710 [In Russian, English summary , p.1710]
Sudakova MI, 1968. Effect of temperature on the life cycle of Aphelenchoides besseyi. Parazitologiya, 2:71-74
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Tamura I, Kegasawa K, 1958. Studies on the ecology of the rice nematode, Aphelenchoides besseyi Christie. II. On the parasitic ability of rice nematodes and their movement into hills. Japanese Journal of Ecology, 8:37-42
Taylor DP, Ngundo BW, Othieno SM, 1972. Outbreaks and new records Tanzania: Rice white tip nematode. FAO Plant Protection Bulletin, 20(2):41-42
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Tikhonova LV, 1974. White tip of rice - a dangerous rice disease. Zashchita Rastenii, 3:32-34
Tikhonova LV, Ivanchenko Yu N, 1968. The combined infection of rice with a fungus, Piricularia and a nematode, Aphelenchus. Trudy Vsesoyuznogo Instituta Gel'mintologii im. K. I. Skryabina, 14:287-290
Timm RW, 1955. The occurrence of Aphelenchoides besseyi Christie, 1942 in deep water paddy of East Pakistan. Pakistan Journal of Science, 7:47-49
Timm RW, 1965. A preliminary survey of the plant parasitic nematodes of Thailand and the Philippines. Bangkok, Thailand: South-East Asian Treaty Organisation, 71 pp
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Todd EH, Atkins JG, 1958. White tip disease of rice. I. Symptoms, laboratory culture of nematodes, and pathogenicity tests. Phytopathology, 48:632-637
Vuong Huu Hai, Rabarijoda P, 1968. Note préliminaire sur la présence des nématodes parasites du riz à Madagascar: Aphelenchoides besseyi Christie 1942, Ditylenchus augustus (Butler 1913) Filipjev 1936. Agronomic Tropicale, Nogent, 23(10):1025-1048
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Distribution References
Ancalmo O, Davis WC, 1962. Diseases of rice in new El Salvador. In: Plant Disease Reporter, 46 (4) 293.
Atkins JG, Todd EH, 1959. White tip disease of rice. III. Yield tests and varietal resistance. In: Phytopathology, 49 189-191.
AVA, 2001. Diagnostic records of the Plant Health Diagnostic Services., Singapore, Plant Health Centre Agri-food & Veterinary Authority.
Barat H, Delassus M, Vuong Huu Hai, 1966. (Présence en Casamance de l'anguillule de feuilles de riz, Aphelenchoides besseyi Christie 1942). In: Agron. Trop, Nogent, 21 (1) 47-55.
Barat H, Delassus M, Vuong Huu, Hai, 1969. The geographical distribution of white tip nematode disease of rice in tropical Africa and Madagascar. In: Nematodes of tropical crops. Technical Comunication Commonwealth Bureau of Helminthology, 40 [ed. by Peachey JE]. 269-273.
CABI, Undated. Compendium record. Wallingford, UK: CABI
CABI, Undated a. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI
Fernandez Diaz Siveira M, 1967. (Lista de nematodes de Cuba). In: Revta Agric. 1 Habana, 74-88.
Javor I, 1970. (A rizsfonálféreg (Aphelenchoides besseyi Christie) hazai felderftésének tapasztalatai). In: Novényvédelem, 6 259-263.
Kermarrec A, Anais A, 1973. (Presencia en Guadeloupe de Aphelenchoides besseyi Christie 1942 (Nematoda, Aphelenchoidae) en follaje del mapney: Dioscorea trifida L). [Comm. V1 Congr. ONTA, Maracay, Venezuela, 1-6 Oct. 1973], 11 pp.
Lordello LGE, 1969. (OcorOncia du nematoide Aphelenchoides besseyi em arroz no Brasil). In: Revta Agric., S. Paolo, 44 (4) 129-131.
Merny G, 1970. (Les nématodes phytoparasites de rizières inondées de la Côte d'Ivoire. I. Les espèces observées). In: Cahiers de l'ORSTOM, Sér. Biol. 11 3-43.
Peachey JE, Larbey DW, Cain SC, 1966. White tip disease of rice in Africa. In: Helminth Abstr. 35 (4) 337-339.
Rahim MAA, 1988. Nematodes associated with paddy seeds in Malaysia Planti-Proceedings 1988, No. 3, 187-199. [Proceedings of the symposium, Movement of pests and control strategies], Kuala Lumpur, Malaysia:
Siddiqi MA, 1970. White tip and ufra disease of rice. In: Plant Pathology Advisory Circular, Malawi: Ministry of Agriculture and Natural Resources. 4 pp.
Stoyanov D, 1979. The nematode fauna of rice in Bulgaria. Rasteniev"dni Nauki. 16 (1), 115-120.
Sudakova IM, Mastennikova VF, Dergunov ID, 1964. Effect of nitrate fertilisers on Aphelenchoides besseyi responsible for 'white tip' disease of rice. In: Zool. Zh. 43 (11) 1708-1710.
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