of tomato have been based primarily onthe use of certified seed and transplants(11,17). However, because of a long incu-bation period and lack of adequatemethods to detect low populations of C.m. michiganensis from infested seed andsymptomless transplants, the diseasecontinues to be a threat. Hence, hostresistance seems to be the most promisingapproach for disease management ifresistance can be incorporated into high-yielding, adapted cultivars. Partialresistance (i.e., tolerance) to C. m.michiganensis has been expressed asreduced severity of symptoms, whichprobably is associated with a lower leveiof systemic infection by C. m. michi-ganensis, and corresponds to lowerreductions in yield (6,19).

ACKNOWLEDGMENTSWe thank D. A. Emmatty, Heinz USA, for advice

and support and M. Hurt, K. Nofftz, R. Paoli, andK. Horn from the University of IlIinois PomologyFarrn, Urbana, for technical assistance.

LITERATURE CITEDI. Bryan, M. K. 1930. Studies on bacterial canker

of tomato. J. Agric. Res. 41:825-851.2. Carlton, W. M., Gleason, M. L., and Braun,

E. J. 1991. Effects of pruning on yield and

disease development in tomato plants support-ing epiphytic populations of Clavibacter michi-ganensis subsp. michiganensis. (Abstr.) Phyto-pathology 81: 1194.

3. Chang, R. J., Ries, S. M., and Pataky, J. K.1991. Dissemination of Clavibacter michigane-nsis subsp. michiganensis by practices used toproduce tomato transplants. Phytopathology81:1276-1281.

4. Dhanvantari, B. N. 1989. Effect of seed extrac-tion methods and seed treatments on controlof tomato bacterial canker. Cano J. Plant Pathol.Ii :400-408.

5. Dullahide, S. R., Moffett, M. L., Heaton, J. B.,and Giles, J. 1983. Effect of time of inoculationof Corynebacterium michiganense subsp. michi-ganense on yield of trellised tomatoes. Aus-traias. Plant Pathol. 12: 15-16.

6. Emmatty, D. A., and John, C. A. 1973.Comparison of yield loss to bacterial canker oftomato in a resistant and a susceptibIe variety.Plant Dis. Rep. 57:787-788.

7. Freebairn, H. T., and Buddenhagen I. W. 1964.Ethylene production by Pseudomonas solana-cearum. Nature 202:313-314.

8. Gitaitis, R. D. 1990. Induction of a hypersen-sitivelike reaction in four-o'clock by Clavibactermichiganensis subsp. michiganensis. Plant Dis.74:58-60.

9. Gitaitis, R. D., Beaver, R. W., and Voloudakis,A. E. 1991. Derection of Clavibacter michi-ganensis subsp, michiganensis in syrnptornlesstomato transplants. Plant Dis. 75:834-838.

10. Goodman, R. N., Kiraly, Z., and Wood, K. R.1986. The Biochemistry and Physiology of PlantDisease. University of Missouri Press, Colurn-bia. 433 pp.

Possible Root Transmission of the Red Ring Nematode(Rhadinaphelenchus cocophilus) to Coconut Palms

lI. Jones, J. B., Stall, R. E., and Zitter, T. A. 1991.Compendium of Tomato Diseases. AmericanPhytopathological Society, SI. Paul, MN. 73 pp.

12. Kennedy, B. W., and Alcorn, S. M. 1980.Estimates of U.S. crop losses to prokaryoteplant pathogens. Plant Dis. 64:674-676.

13. McKeen, C. D. 1973. Occurrence, epidemiology,and control of bacterial canker of tomato insouthwestern Ontario. Cano Plant Dis. Surv.53: 127-130.

14. Ricker, M. D., and Riedel, R. M. 1988.Economic importance of secondary spread ofClavibacter michiganensis subsp. michiganen-sis in northern-grown processing tomatoes.(Abstr.) Phytopathology 78: 1570.

15. Sequeira, L. 1973. Hormone metabolism indiseased plants. Annu. Rev. Plant Physiol.24:353-380.

16. Sherf, A. F., and Macnab, A. A. 1986. VegetableDiseases and Their Control. 2nd ed. J ohn Wiley& Sons, Inc., New York. 728 pp.

17. Strider, D. L. 1969. Bacterial canker of tomatocaused by Corynebucterium michiganense. Aliterature review and bibliography. N.C. Agric.Exp. Stn. Tech. BulI. 193. 110 pp.

18. Suparyono, and Pataky, J. K. 1989. Relation-ships between incidence and severity ofStewart'sand Goss's bacterial wilts and yield of sweetcorn hybrids. Crop Prol. 8:363-368.

19. Thyr, B. D. 1968. Resistance to bacterial cankerin tomato, and its evaluation. Phytopathology58:279-281.

20. Weller, D. M., and Saettler, A. W. 1978.Rifampin-resistant Xanthomonas phaseoli var.fuscans and Xanthomonas phaseoli: Tools forfield study of bean blight bacteria. Phytopath-ology 68:778-781.

DULCE R. N. WARWICK and A. P. T. BEZERRA, National Center for Coconut Research Embrapa, CP 44,Aracaju, SE 49000, Brazil

ABSTRACTWarwick, D. R. N., and Bezerra, A. P. T. 1992. Possible root transmission of the red ringnematode t Rhadinaphelenchus cocophilus) to coconut palms. Plant Dis. 76:809-811.

The significance of root transmission of the red ring nematode (Rhadinaphelenchus cocophilus)to coconut palms (Cocos nucifera) was investigated in a screen-house experiment. Transmissionby root contact occurred in seven of 15 plants growing araund five inoculated plants. In anotherexperiment, each plant became infected when a nematode suspension was placed on the mecha-nically damaged roots. Young seedlings planted in a hole where previously diseased palmswere growing did not develop the typical symptoms of red ring disease. Red ring nematodescould not successfully colonize the husk tissue or the bole area. Seedlings were also artificiallyinfected with red ring nematodes and observed for 30 wk. Nematodes could be extracted framthe seed of only one plant. At the end of the 30-wk period, no nematodes could be detected.Thus, seedling tissue may not be suitable for development of red ring nematodes.

Red ring disease of coconuts, causedby Rhadinaphelenchus cocophilus (Cobb)Goodey, leads to severe losses in coconut(Cocos nucifera L.) plantations through-out tropical America (4,14,15,19). Coco-nut trees of 3-10 yr are most affected

Accepted for publication 12 December 1991.

This article is in the public domain and not copy-rightable. It may be Ireely reprinted with cus-tomary crediting 01 the source. The AmericanPhytopathological Society, 1992.

(17). Typical internal symptoms of thedisease include a brown-orange (red) andyellow ring in cross section; this ring isthe main characteristic of the d isease.Young leaves are ais o discolored, and thewhole plant collapses in the course ofdisease development. No shedding ofnuts occurs in any stage. The red ringis 2-4 em wide and is located about 5em from the edge of the stem. The dis-colored area is largely infested and con-tains a high number of active nematodes.

The transmission of the red ring nema-tode by the palm weevil Rhynchophoruspalmarum L. (Coleoptera, Curculioni-dae) is well-documented (3, 11,12). Thefirst evidence that the palm weevil wasa vector of red ring disease was suppliedby Cobb (3). Hagley (11) examined 157palms and found that 95% of the palmswith red ring disease were ais o infestedwith weevils. He also examined 213 field-collected weevils and found that 38.5%of the field population was externallycontaminated with living nematodes.Later, Hagley (12) reported that theincidence of red ring disease was highlycorrelated with the seasonal abundanceof the palm weeviI. Gerber and Giblin-Oavis (8) reported that more than 90%of newly emerged weevil adults in Trini-dad are infested with red ring nematodes.Griffith (10) concluded that the controlof the disease could be best achieved bysanitation measures and vector controI.

Studies on direct transmission of thenematode through the palm roots in thefield are difficult, because there is alwaysthe chance of nematode transmission by

Plant Disease/August 1992 809

the palm weevil. Blair (I) conducted in-oculation experiments and found thatroots became infested when inoculatedwith a water suspension ofthe nematode.Goberdhan (9) also demonstrated thatartificial infection is possible through theintroduction of fragments of nematode-infected tis sue. Kastelein (13) indicatedthat the red ring nematode might ais ooccur in soi!. Franco (7) found that thenematode is transmitted through rootcontact in cases in which the red ringdevelops from the bottom to the top ofthe palm.

The purpose of this study was to deter-mine if direct transmission ofthe red ringnematode occurs through root contact

and cultivation practices. The possibilityof transmission to young seedlings andseedling susceptibility were also investi-gated. The experiments were done in ascreen house, where the presence of R.palmarum was neve r observed.

MATERIALS AND METHODSRoot transmission test. Twenty

healthy coconut seedlings of cultivar Bra-zil Tall were obtained from an area freeof red ring disease and were transplantedin a screen house in 1987. The exper-iments were done 3 yr later, when plantsbegan to form boles and were susceptibleto the nematode (17). Red ring nema-todes were obtained from infected tis sue

• -.19

.2 e e -14 -18

• .1 e ·9 .13 .17

• • • •Fig. l. Map of the locations (in the screen house) of the 20 coconut palms used in the roottransmission experiment. Plants 5, 6, 10, 11, and 12 were mechanically inoculated in the stemwith Rhadinaphelenchus cocophilus.

Table l. Number of active red ring nematodes C Rhadinaphelenchus cocophilus) found in coconuttissue

Number of nematodes per gram of tissue

Weeks after Stem (em above soilline)

Plant number' inoeulation Roots 5 30 60 90I 302 17 5 343 304 305" 7 156 376 136 76" 7 20 1897 13 8 52 178 309 21 108 381 97 15 6

10" 7 18 71 183 9711" 7 152 17812" 7 23 18913 30 51 78 41 23 6514 12 23 1215 30 4 4 4 8016 1217 3018 3019 3020 30 19 82 19 47 75

'**, Plants artificially inoculated with nematode suspension.b No nematodes found.

810 Plant Disease/Vol. 76 No. 8

•

(4). A suspension (5 ml) contai.\\i.\\~ l.iTproximately 6,000 nematodes was intro-duced into the base of the stem of fiveplants; a drill and a hypodermic syringewere used. To determine if the leavesshowed external symptoms of yellowing,we observed the remaining 15 plants,which grew around the infected ones(Fig. I). When any symptoms were ob-served, the plant was uprooted and sam-pled. The remaining nonsymptomaticplants were removed 30 wk later, at theend of the experiment.

CuItivation testo In another trial, 12coconut plants of the same cultivar andage as those used in the root transmissiontest were cultivated with a hoe. A sus-pension of active nematodes (3,000 nem-atodes per liter ofwater) was poured overthe damaged roots. The soil in the sur-rounding area was watered and keptmoist for 2 days. This work was ais o donein the screen house, where R. palmarumwas not present.

Seedling susceptibility. We cond uctedthe experiment to determine if seedlingsplanted into sites where infected plantshad been removed would become in-fected with red ring. Immediately afterthe infected plant was taken out, 10 seed-lings of the coconut cultivar CameroonRed Dwarf, each 7 mo old, were plantedin the same hole without chemical treat-ment. After I or 2 mo, the plants wereremoved and examined for the presenceof red ring nematodes. This experimentwas also done in the screen house, freefrom the presence of R. palmarum. Seed-ling susceptibility was further investi-gated by mechanical inoculation of 20palms. A suspension (5 ml) containing3,000 nematodes was introduced into ahole made by a drill at the base and intothe stem. In every test, the plantingdensity was 294 trees per hectare.

Sampling and processing. Pieces ofroot tissue (2 em long) and pieces of stemtissue (50 g) were taken at stem heightsof 5, 30, 60, and 90 em, starting at thesoil line, and the number of nematodesper gram of tissue was determined. Inali cases, the plants were observed forexternal symptoms and then removed.In the laboratory, we examined samplesfor nematodes following the standardprocedure (5).

RESULTSRoot transmission. The five trees

subjected to basal mechanical inocula-tion developed symptoms of leaf yel-lowing within 7 wk. Nematodes werefound in the bole area of ali inoculatedplants (Table I). Nematodes were de-tected in seven of the 15 plants surround-ing the five mechanically inoculatedplants (Table I). Nematodes were de-tected in the uninoculated plants 12 wkafter the first mechanical inoculation(plant 14). Again, nematodes were foundin the roots, bole area, and 30 em abovethe soil line. At week 17, the nematode

was found only in the bottom part ofplant 2. ln plant 9, cut 21 wk after thefirst inoculation, nematodes had invadedthe whole stem (Table I). After 30 wk,clearly visible leaf symptoms indicatedthat the plants were succumbing to redring disease. When plants 13, 15, and 20were examined, nematodes had invadedthe stems and the roots (Table I). Thenumber of nematodes per gram of planttissue ranged from 4 to 381. More nema-todes were found in the mechanicallyinoculated plants than in the plants inwhich the nematodes were presumablyacquired through root contact.

Cultivation testo Ali 12 plants that weresubjected to root damage and wateredwith a nematode suspension developedsymptoms at between 80 and 92 days.By this time, red ring infection was welladvanced. The oldest and lowest threeleaves had died, and the other leaves wereyellowing progressively. When theseplants were cut apart and examined,nematodes were found throughout thestems. Leaf yellowing was not observedin two plants, although nematodes wereextracted from the roots and the stemtissue from up to 30 em.

Seedling susceptibility. Seedlings thatwere replanted after diseased plants wereremoved remained healthy. No nema-todes were detected in the roots, stemregion, or in the old seed. Twenty youngseedlings that were inoculated mechani-cally did not develop the disease either;however, six red ring nematodes wereextracted from one seedling.

DISCUSSIONThe recommended density of 143 tall

coconuts per hectare posed problems fordoing transmission experiments. ln ourexperiment, a spacing of 3 m betweenplants and a density of 294 trees perhectare was used, and nematode trans-mission by root contact with infectedplants to healthy ones occun ed in theexperiment. However, in a coconut plan-tation, root contact occurs constantly.Menon and Pandalai (16) measured alength of 22 m for a single root. ln addi-

tion, when trees are replanted, the com-mon practice is to plant the new treesbetween the old rows with a 4-m spacebetween plants.

Schuiling and Van Dinther (18)showed that a nematode population wasfound almost exclusively in the necroticarea of the ring. The number of nema-todes extracted ranged from O to 4,833per gram of tissue; the average was 300per gram of tissue. ln our trial, the num-ber of nematodes was lower and rangedfrom O to 381. This may be explainedby the young age of the plants used inthe experiment. The number of activenematodes varied enormously in thesamples and among the plants. However,on the average, mechanically infectedplants showed symptoms first and hadmore nematodes than the plants thatbecame infected through root contact.This was expected, because the numberof nematodes in inoculated plants isprobably higher (6,000) than in plantsto which nematodes migrated from dis-eased plants.

Results similar to those in previousexperiments with red ring disease wereobtained with seedlings (6). We suggestthat seedling tissues are not suitable forthe development of nematodes. Accord-ing to Blair (1,2), green nuts can supportnematode populations when the nuts areinoculated artificially, but nematodescannot pass through the fruit stalk whenthe nuts are inoculated on a bearing tree.ln our study, the seedlings were not sue-cessfully colonized, and no nematodeswere recovered from them, except in onecase after mechanical inoculation.

ln conclusion, red ring nematodes canbe transmitted by means other than theinsect vector. lnfected plants should beremoved immediately if by doing so fur-ther root contact can be avoided. Wound-ing of roots during cultivation practicesshould also be avoided.

L1TERATURE CITEDI. Blair. G. P. 1963. Red ringdiseaseofthecoconut

palmo J. Agric. Soe. Trinidad & Tobago 64:31-49.2. Blair, G. P. 1965. The use of immature nuts

of Cocos n u cifer a for studies on

Rhadinaphelenchus cocophilus. NematologicaII :590-592.

3. Cobb, N. A. 1922. A note on the coconutnematode of Panama. J. Parasitol. 9:44-45.

4. Dean, C. G., and Velis, M. 1976. Differencesin the effects of red ring disease on coconutpalms in Central America and the Caribbeanand its control. Oléagineux 31:321-324.

5. Fenwick, D. W., and Maharajis. 1963. Recoveryof Rhadinaphelenchus cocophilus (Cobb, 1919),Goodey, 1960 from coconut tissues. J. Hel-minthol. 37: 11-14.

6. Fenwick, D. W., and Mohammed, S. 1964. Arti-ficial infections of seednuts and young seedlingsof the coconut palm with the red ring nematodeRhadinaphelenchus cocophilus (Cobb).Nematologica 10:459-463.

7. Franco, E. 1964. Estudo sobre o anel-vermelhodo coqueiro. Aracaju, Inspetoria de Defesa San-itária Vegetal. 236 pp.

8. Gerber, K., and Giblin-Davis, R. M. 1990.Association of the red ring nematode and othernematode species with the palm weevil, Rhyn-chophorus palmarum. J. Nematol. 22:143-149.

9. Goberdhan, B. 1964. Observations on coconutpalms artificially infected by the nematodeRhadinaphelenchus cocophilus (Cobb, 1919)Goodey, 1960. J. Helminthol. 38:25-30.

10. Griffith, R. 1979. Patterns of control in red ringdisease. FAO Tech. Work. Party CoconutPr oduct. Prol. Processo 5th.

11. Hagley, E. A. C. 1962. The palm weevil Rhyn-chophorus palmarum L., a probable vector ofred ring disease of coconuts. N ature (London)193:499.

12. Hagley, E. A. C. 1963. The role of the palmweevil Rhynchophorus palmarum as a vectorof red ring disease of coconuts. I. Results ofpreliminary investigations. J. Econ. Entomol.56:375-380.

13. Kastelein, P. 1986. Observations on red ringdisease of coconut palms in Suriname. Suri-naamse Lanabouw 34:40-53.

14. Kraaijenga, D. A., and Den Ouden, H. 1966.Red ring disease in Surinam. Neth. J. PlantPathol. 72:20-27.

15. Lordello, L. G. E., and Zamithe, A. P. L. 1954.Constatação da moléstia do "anel vermelho" docoqueiro no Estado do Rio de Janeiro. Redis-crição do agente causador Aphelenchoidescocophilus (Cobb, 1919) Goodey, 1933 (Nema-toda aphelenchidae). An. Esc. Super. Agric.Luiz de Queiroz-Piracicaba 11: 125-132.

16. Menon, K. P. V., and Pandalai, K. M. 1958.The coconut palm: a monograph. Indian Cent.Coconut Comm. Ernakulam.

17. Ohler, J. G. 1984. Coconut tree of life. FAOPlant Prol. Papo 57). 446 pp.

18. Schuiling, M., and Van Dinther, J. B. M. 1982.La maladie de I'anneau rouge à Ia plantationde palmiers à huile de Paricatuba, Para (Brésil).Une étude de caso Oléagineux 37:555-563.

19. Singh, N. D. 1972. A survey of red ring diseaseof coconut palm in Grenada, West Indies. PlantDis. Rep. 56:339-341.

Plant Disease/August 1992 811