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Pest Description
Red Ring Disease of Coconut
IDENTITY:  Scientific name: Bursaphelenchus cocophilus (Cobb) Baujard 1989.
Synonym: Rhadinaphelenchus cocophi1us (Cobb 1919) J.B. Goodey 1960.
(Note: Hunt (1993) considers Rhadinaphelenchus cocophi1us a valid scientific name.
However, the results of DNA analysis conducted by the first author support
Baujardís proposal to consider the genus Radinaphelenchus a junior synonym of Bursaphelenchus)
Common name: Red ring nematode

Fact Sheet prepared by: Robin M. Giblin-Davis, Paul S. Lehman, and Renato N. Inserra

JUSTIFICATION:  Bursaphelenchus cocophi1us causes the lethal red ring disease of palms. Palms are important landscape plants in subtropical areas of the United States and the introduction of this nematode would cause great concern for the landscape and tourism industries.

WORLD DISTRIBUTION:  Belize, Brazil, Colombia, Costa Rica, Ecuador, El Salvador, French Guiana, Grenada, Guatemala, Guyana,  Honduras, Mexico, Nicaragua, Panama, Peru, Saint Vincent and the Grenadines, Suriname, Trinidad and Tobago, and Venezuela. Although the nematode has been reported to be present in Barbados, Dominica, and Jamaica, these reports have not been confirmed, and EPPO considers it to be absent from these countries. The nematode has not been reported in the continental US, Virgin Islands, or Hawaii.  CAB International (2002) reports B. cocophilus in Puerto Rico, however, recent surveys for the red ring nematode in Puerto Rico negated this report (José Chavarria, University of Puerto Rico, Mayagüez, personal communication). Although some sources report that the nematode is present in the Bahamas, Dominican Republic, and Haiti, this is questionable and requires confirmation.

HOST PLANTS:  Hosts of B. cocophilus are confined to the family Palmae where the nematode is known to infect over 17 species. Most palm species appear to be susceptible to inoculation by red ring nematode but disease severity and symptoms are variable. The most economically important species with red ring disease susceptibility are coconut palm, Cocos nucifera L., the African oil palm, Elaeis guineensis Jacquin, and the date palm, Phoenix dactylifera L.  Under greenhouse conditions, West Indian royal palm (Roystonea oleracea), gru-gru palm (Acrocomia aculeata), Moriche palms (Mauritia flexuosa), and cucurite palm (Maximiliana maripa) were infected artificially.

ECONOMIC DAMAGES:  This nematode causes serious damage to coconut and oil palms, which are stunted and eventually killed by the nematode infection. Red ring disease is one of the most important wilt diseases of coconut palm and African oil palms in the Neotropics causing up to 10-15% annual losses.

BIOLOGY AND LIFE CYCLE:   Bursaphelenchus cocophi1us is associated with the palm weevil, Rhynchophorus pa1marum which transmits it to the coconut palm, Cocos nucifera and the African oil palm, E1aeis guineensis. The red ring nematode is co-distributed with the palm weevil in the lower Antilles, and Mexico southward into South America.  Reports of detection of R. palmarum in Texas and California have not been substantiated by recent survey results (M. Thomas, personal communication). A schematic drawing of the association of B. cocophi1us with its weevil and coconut hosts is presented in Figure 1.  Adu1t females, which are internally infested by B. cocophi1us, disperse the dauer juvenile nematodes to healthy coconut palms and deposit the juvenile stage of the nematode during oviposition, usually at the leaf axils or internodes. Nematodes enter oviposition wounds, feed, and reproduce in the palm tissues, causing the death of the infected trees. The weevil larvae are associated with as many as 10,000 juveniles of B. cocophi1us,which persist in the insect through metamorphosis, apparently without molting, and appear to aggregate around the genital capsule of the adult weevil.   The adult weevils emerge from their cocoons in the rotted palm and disperse to apparently healthy or stressed and dying palms, completing the life cycle.   Other beetles, Dynamis borassi [F.] and Metamasius hemipterus [L.] are also reported to vector the red ring nematode.

The rate of disease development is affected by the host palm species, age, and other factors.  The first clear internal symptom in C. nucifera is a red ring in the stem that occupies about 70 cm around the inoculation point and occurs between 14 and 21 days post-inoculation.  The first external symptoms occur at about 28 days post-inoculation and include leaf yellowing in two to three of the older leaves and premature death of the oldest leaf.  The first external symptoms occur in about 30 days regardless of whether the inoculation is made in a wound at the stem base or just below the crown.  At 42 days, the entire stem is infected with B. cocophilus at close to peak population levels and some of the petioles and roots are infested with nematodes.  Bursaphelenchus cocophilus occurs intercellularly in the ground parenchymal cells adjacent to and within the red ring in the stem, discolored tissue in the petioles, and in the cortex of the roots.  Red ring nematodes do not occur in the xylem or phloem tissues, but xylem vessels become occluded with tyloses where they pass through the red ring.  Physical damage caused by nematode feeding compromises the storage capacity and energy dynamics of the palm host and vascular occlusion prevents normal water relations.
Experimental inoculations into nuts on inflorescences or onto unwounded stems of coconut do not lead to red ring disease.  Inoculations onto wounded or unwounded roots of 3-7 year-old coconut palms do lead to red ring disease.  Infested root to healthy root transmission and contamination of wounds in healthy coconut by red ring nematodes carried on the body or feces of R. palmarum are occasional modes for the spread of red ring disease.  However, B. cocophilus inoculation by internally infested R. palmarum females during oviposition into healthy, pruned, or wounded palms is probably the most common route for transmission. In a study in Trinidad, over 47% of newly-emerged adult R. palmarum from red ring-diseased coconut palms were internally infested with more than 1,000 dauer juveniles of B. cocophilus.

DAMAGE SIGNS AND SYMPTOMS:  Symptoms of red ring disease vary widely with palm species and age, cultivar, and environmental conditions.  Palms younger than 2.5 years old cannot be experimentally infected with B. cocophilus and red ring disease has not been recorded from palms of this age in the field. Host specific differences in symptoms were consistent in both coconut and African oil palms in cross inoculations, regardless of the host of inoculum origin.
  In C. nucifera, classical red ring symptoms include premature nut fall (except for mature nuts), withering of inflorescences, and yellowing, bronzing, and death of progressively younger leaves.  Yellowing of leaves usually starts at the tips of the pinnae and moves inward to the rachis and then to the base of the petiole.  Several of the dying or dead leaves will often break close to the petiole and remain hanging from the stem.  A stem transverse section will reveal a discrete brick to brownish-red ring that is 2-6 cm wide and occurs 2-6 cm within the stem periphery.  The leaf petioles and cortex of roots can also be discolored yellow to brownish-red.  In longitudinal section, discoloration is usually continuous throughout the length of the stem, appearing as two bands that unite at the base and form discontinuous lesions near the crown.  In African oil palm, classical symptoms involve progressive premature yellowing and death of older leaves that break at the petiole and hang.  Stem transverse sections reveal a brown, cream, or rose-colored ring that is a few centimeters wide and is concentric to the periphery of the stem.  Irregular-shaped rings and rings that are not continuous through the stem are common.
Coconut palms 3-10 years-old and African oil palms older than 5 years-old usually die within 2-4 months of infection.  Severe damage to the crown of red ring-diseased coconut palms is caused by larval feeding of the large weevil vector, R. palmarum. Older coconut palms (> 20 years old) have been reported with red ring disease displaying less definitive symptoms with a more prolonged death.  Dauer juveniles can be harvested from the discolored tissue of the ring from coconut (up to 11,000 nematodes/g of tissue), from leaf petioles, or roots to confirm disease diagnosis from symptoms. Nematode recovery from African oil palms is highly variable.
Chronic little leaf symptoms caused by B. cocophilus have also been reported for coconut palms, especially in older trees.  Coconut palms begin abnormal production of very short leaves which give crowns the unusual appearance of a feather duster. As the disease progresses, there can be a decrease in leaf size and surface area to the point where the leaf is reduced to a leafless rachis with suberized lesions over most of its surface.  New leaves and inflorescences are aborted and palms become unproductive.   Red ring nematodes can be recovered from necrotic lesions in the middle and distal parts of unpresented leaves. Little leaf and a combination of red ring and little leaf symptoms can be more common in African oil palms.

DIAGNOSIS OR IDENTIFICATION:  Females and males of B. cocophilus are 60-139 and 65-179 times longer than wide, respectively, with the greatest body width being less than 15.5 um and total length ranging from 775-965 um from little leaf symptomatic African oil palm and 812-1369 um from coconut or African oil palms with typical red ring symptoms.  The metacorpus and stylet in the second-stage juveniles and adults are well developed. Stylet length is between 11-15 um in adults.  Females have a vulval flap which appears bowed posteriorly when viewed ventrally, a long post-uterine sac (extending about 75% of the vulva-anal distance), and an elongate tail (62-117 um ) with a rounded terminus.  Males have seven caudal papillae; one ventral preanal papilla, one pair of subventral preanal or adanal papillae, and two pairs of subventral postanal papillae.  The distal ends of the spicules in the males are heavily sclerotized and the caudal alae form a spade-shaped flap (= bursal flap).  Third-stage dauer juveniles from coconut palm usually range from 700-920 um and have a pointed tail with or without a mucron.  The metacorpus is usually not well developed in dauer juveniles from the palm or the weevil vector and the stylet is not visible.  Survival of dauer juveniles of B. cocophilus is very poor under unsterile conditions in soil or water at room temperature or in the refrigerator (100% mortality in < 7 days).  Survival can be prolonged for 70-80 days at room temperature when nematodes are surface-sterilized and stored in autoclaved red ring nematode-diseased stem tissue extract (R) or R plus D-glucose or lactose.
Red ring nematodes can be inoculated into and cultured in coconut palms older than 2.5 years old, in husks of nearly mature coconut fruits, or in exised leaf stalks (leaf 6 to 13 on a nut-bearing coconut palm) which has been trimmed of the pinnae and the cut ends have been paraffin coated.  Cultures in immature fruits or leaf stalks must be subcultured about once every 4 weeks.

ERADICATION/SUPPRESSION MANAGEMENT STRATEGIES:  Phytosanitation is still the best method of red ring disease management.  This strategy is directed at reducing the vector population as well as the number of sources for nematode inoculum. As soon as palms with red ring disease or B. cocophilus-induced little leaf symptoms have been detected they should be destroyed.  In coconut palm, the disease can be confirmed by examining stem tissue extracted with a coring device for evidence of discoloured tissue and red ring nematodes.  In African oil palm, stem coring for evidence of necrosis and red ring nematodes is not reliable.  Trees should be sprayed with an insecticide (ie. methomyl) and killed with 100-150 mls (48.3% a.i.) of the herbicide monosodium acid methanearsonate (MSMA) or other herbicide that is injected or placed into the trunk.  Occasionally trees injected with MSMA will harbor weevil larvae.  Therefore, the tree should be cut and sectioned to make sure that weevils are not present.  Palms that are heavily infested with weevils should be cut, sectioned, and treated with an insecticide such as methomyl, trichlorfon, monocrotophos, carbofuran, cabaryl, or lindane.  Injections of systemic nematicides, such as fenamiphos, oxamyl, and carbofuran into little leaf symptomatic palms can help with palm recovery.  However, because of the damage to the very young leaves in little leaf palms the recovery can take between 6-8 months.

Recent research in African oil palm plantations suggests that concerted aggressive phytosanitation and mass-trapping with traps baited with sugarcane and synthetic aggregation pheromone (Rhyncholure; racemic 6-methyl-2-hepten-4-ol; ChemTica International) reduce the numbers of R. palmarum and change their distribution patterns (from highly aggregated to random) while reducing red ring disease incidence. At mass trapping onset, most R. palmarum were captured in "border" traps of the test site suggesting removal of potential immigrants into the study area.  A combination of perimeter and "internal" traps is most effective for mass trapping.  More than 62,500 weevils (?94 weevils per ha per month) were captured during one study, with red ring disease incidence decreasing by a factor of > 2.

RESEARCH NEEDS:  It is important to determine if R. cruentatus, which is endemic to southeastern USA is able to vector the red ring nematode on economically important palms. There is a need for systematic periodic surveys for B. cocophilus in the Caribbean and South American countries where the nematode is not known to be present, especially in Jamaica, which is a source of certified seednuts. Palm weevil pheromones should allow for determining weevil vector presence and red ring nematode contamination at ports of entry in countries without R. palmarum and/or B. cocophilus and could be useful in settling disputed claims of weevil and/or red ring nematode presence in countries such as the Bahamas, Jamaica, Puerto Rico, Dominican Republic, and Haiti.

KEY SCIENTIFIC CONTACTS:  Robin M. Giblin-Davis, Ft. Lauderdale Research & Education Center, IFAS, University  of Florida, 3205 College Ave., Ft. Lauderdale, FL 33314.

Baujard, P. 1989. Remarques sur les genres des sous-familles Bursaphelenchidae Paramanov, 1964 et Radinaphelenchinae Pramanov, 1964 (Nematoda: Aphelenchoididae). Revue de Nématologie 12:323-324.
Brathwaite, C. W. D. and M. R. Siddiqi. 1975. Rhadinaphelenchus cocophilus. C.I.H. Description of Plant Parasitic Nematodes, Set 5, No. 72.
Chinchilla, C. 1988. El Sindrome del anillo rojo-hoja pequeña en palma aceitera y cocotero. Boletin Technico  2:113-136.
Dean, C. G. 1979.  Red ring disease of Cocos nucifera L. caused by   Rhadinaphelenchus cocophilus (Cobb, 1919) Goodey, 1960. An annotated bibliography and review.  Technical Communication No. 47 of Commonwealth Inst. Helminthol. 70 pp.
 Esser, R. P.  and J.A. Meredith 1987.  Red ring nematode. Fla. Dept. Agric.& Consumer Serv., Div. Plant Ind., Nema. Circ. No. 141.
Gerber, K. and R. M. Giblin-Davis. 1990. Association of the red ring nematode, Rhadinaphelenchus cocophilus, and other nematode species with Rhynchophorus palmarum (Coleoptera: Curculionidae).  J. Nematol. 22: 143-149.
Gerber, K., R. M. Giblin-Davis, R. Griffith, J. Escobar-Goyes, and A. D'Ascoli Cartaya. 1989.  Morphometric comparisons of geographic and host isolates of the red ring nematode, Rhadinaphelenchus cocophilus. Nematropica 19: 151-159.
Giblin-Davis, R. M. 1990.The red ring nematode and its vectors. Fla. Dept. Agric.& Consumer Serv., Div. Plant Ind., Nema. Circ. No. 181.
Giblin-Davis, R. M., K. Gerber, and R. Griffith. 1989. In vivo and in vitro culture of the red ring nematode, Rhadinaphelenchus cocophilus. Nematropica 19: 135-142.
Giblin-Davis, R. M., M. Mundo-Ocampo, J. G. Baldwin, K. Gerber, and R. Griffith.