PLANT-PARASITIC NEMATODES OF BANANA IN AMERICAN SAMOA
F. E. Brooks American Samoa Community College Land Grant Program, P.O. Box 5319, Pago Pago, American Sa- moa 96799.
ABSTRACT
Brooks, F. E. 2004. Plant-parasitic nematodes of banana in American Samoa. Nematropica 34:65-72. Sixteen commercial banana farms in American Samoa growing the cultivar Williams (Musa AAA, Cavendish subgroup) and eight non-commercial farms with mixed varieties were surveyed over a 10- month period. Fields were assessed for nematode species present, population densities, and root dam- age. In addition, two FHIA hybrids with putative resistance to the burrowing nematode, Radopholus si- milis, were evaluated. Population densities of Helicotylenchus multicinctus and H. dihystera were five times higher, on average, than population densities of R. similis. Pratylenchus loosi and P. gibbicaudatus are new records for American Samoa and this is only the second report of P. gibbicaudatus on Musa spp. The FHIA-01 hybrid had 60 times fewer burrowing nematodes than ‘Williams’ growing in the same field and FHIA-25 had the lowest nematode population densities (all species) of any variety surveyed. Aver- age estimates of external and cortical root necrosis in the commercial fields were both 26%. Key words: American Samoa, banana root damage assessments, FHIA hybrids, Helicotylenchus, Musa, Pratylenchus gibbicaudatus, Pratylenchus loosi, Radopholus similis.
RESUMEN
Brooks, F. E. 2004. Nemátodos parasíticos de plantas en banano en Samoa Americana. Nematropica 34:65-72. Dieciséis fincas bananeras comerciales en Samoa Americana que cultivan el cultivar Williams (Musa AAA, subgrupo Cavendish) y ocho fincas no-comerciales con variedades mixtas fueron hechas un muestreo durante un periodo de diez meses. Campos fueron asesorados por las especies presentes de nemátodos, densidades de poblaciones, y daño a las raíces. Adicionalmente, dos híbridos de FHIA con resistencia aparente al nemátodo barrenador, Radophulus similis fueron evaluados. Las den- sidades de poblaciones de Helicotylenchus multicinctus y H. dihystera eran de un promedio de cinco vec- es más altas que las densidades de población de R. similis, Pratylenchus loosi y P. gibbicaudatus en Musa spp. El híbrido FHIA-01 tenía 60 veces menos nemátodos barrenadores que ‘Williams’ en el mismo campo, y FHIA-25 tenía la población más baja de todas las especies en cualquier variedad asesorada. Ambas stimaciones promedias de necrosis externa y necrosis del cortex de las raíces en los campos comerciales eran 26%. Palabras clave: Samoa Americana, asesorías de daño a las raíces del banano, híbridos FHIA, Helicoty- lenchus, Musa, Pratylenchus gibbicaudatus, Pratylenchus loosi, Radopholus similis.
INTRODUCTION (Radopholus similis (Cobb) Thorne) and spiral (Helicotylenchus multicinctus (Cobb) Five species of plant-parasitic nema- Golden) nematodes, were reportedly caus- todes have been listed on bananas (Musa ing serious root damage and assumed to spp.) in the U.S. Territory of American be suppressing yield. Burrowing and spiral Samoa (Firman, 1975; Grandison, 1996). nematodes are a worldwide problem in These nematodes, especially burrowing banana growing regions causing yield
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losses of 30-50% in Costa Rica and Pan- rado, 1986; Bridge, 1988; Fogain and ama, 40% in Africa, and 30-60% in India Gowen, 1997; Araya et al., 1999). Top-heavy (Davide, 1995). Severe nematode damage banana plants may fall over (topple) at to banana crops has also been reported in fruiting or during strong winds due to the Southeast Asia and all other South Pacific loss of anchoring roots (Gowen, 1995; Islands, including the neighboring inde- Whitehead, 1998), a common sight in pendent nation of Samoa (Siddiqi, 1973; American Samoa. Farmers may incorrectly Bridge, 1988; Davide, 1995). attribute these problems to poor root Banana ranks fourth of all agricultural development, lack of soil nutrients, shal- crops produced worldwide and first among low soil, or unsuitable soil moisture. fruits, with annual sales of approximately Most growers are unaware that nema- US$2.5 billion (Ploetz, 2001). This figure todes are a cause of banana production represents only about 10% of the 78.2 mil- problems and it is important to inform lion tonnes (86 million tons) cultivated. them of possible management options. The remaining 90% is produced by subsis- Only a few nematode management prac- tence farmers and consumed by their fami- tices are available to Pacific Island banana lies. These growers are situated in the farmers in a sustainable system, however, developing tropical regions of Africa, Asia, and some may not be economically or the Americas, and South Pacific. Banana environmentally acceptable (Speijer and and taro (Colocasia esculenta (L.) Schott) Ssango, 1999). are the principle crops grown for market The objectives of this study were to in American Samoa. In 1998, American identify nematodes extracted from banana Samoan growers produced 9.8 million kg roots and soil and estimate their popula- (21.5 million pounds) of ‘Williams’ (Musa tion densities, assess root health, evaluate AAA, Cavendish subgroup) with an esti- banana cultivars with putative resistance to mated value of US$12.5 million (National the burrowing nematode, and suggest Agricultural Statistics Service, 1999). A methods of control. similar amount of bananas from other cul- tivars were produced, such as ‘Misi Luki’ MATERIALS AND METHODS (Musa AAB, Mysore subgroup) and ‘Pata Samoa’ (Musa ABB, Bluggoe subgroup) Survey Method (Daniells, 1995; Jones, 2000), and were val- ued at US$10.5 million. All of these locally Sixteen commercial banana farms and produced bananas are sold and consumed eight non-commercial plantings were sur- on the islands where they were grown. veyed for plant-parasitic nematodes be- Banana is a perennial crop that is tween July 2002 and May 2003 on Tutuila, grown on the same site for many years. the main island of American Samoa. Tu- This practice provides conditions for nem- tuila is located at 14°18’S latitude and atode survival and population increase. 170°41’W longitude. Most soils on these Roots damaged by nematodes are ineffi- farms are well-drained clay loams of either cient in water and nutrient uptake. The the Iliili Series (Medial-skeletal, isohyper- consequences of this damage are a thermic Lithic Dystrandepts) or Oloava reduced rate of plant growth, lengthening Series (Medial over cindery, isohyperther- of the vegetative cycle, suppression of mic Typic Dystrandepts), with an average bunch weights, and a reduction in the pro- effective rooting depth of 90 cm (35-150 ductive life of the farm (McSorley and Par- cm) (Soil Conservation Service, 1984). Av-
Plant-parasitic nematodes of banana: Brooks 67
erage annual rainfall is 400 cm per year spiral nematode and expressed them as (300-625 cm) over these sites, with a mean coalesced lesions extending to the stele. annual temperature of 26°C. Commercial farms selected for the sur- Nematode Extraction vey grew only ‘Williams’. Ten plants in The method of extraction was based on their first 14 days of flower emergence the procedures described by Hooper (Sarah, 1993; Speijer and Gold, 1995) were (1990) and Speijer and Ssango (1999). The arbitrarily chosen for sampling. From each 5 root pieces assessed for cortical necrosis plant, all banana roots and approximately were cut into 1-cm-long segments and 100 g of soil were removed from holes mea- mixed. A 5-g subsample was then added to suring 25 cm on a side dug next to the base 50 ml water and blended at medium speed of the rhizome. The roots of each plant for 10 seconds. The macerate was poured were kept separate and placed into individ- onto two 2-ply layers of paper toweling ual plastic bags, but soil from the 10 plants (Bounty, Procter and Gamble, Cincinnati, was mixed into a bulk sample (Speijer and OH) suspended on a Baermann tray with Gold, 1995; Fogain and Gowen, 1997; the water level in the tray touching the Araya et al., 1999). Sampling methods were roots (McSorley, 1987). Two days later the the same in the non-commercial fields. In water was removed, replaced with fresh order to sample plants at the same growth water, and the nematodes counted in two stage on the same cultivar on these private 2.5 ml aliquots of the suspension. Changing farms, fewer than 10 plants were sampled. water during incubation increased extrac- Two tetraploid hybrids resistant to black tion efficiency (Brooks, personal observa- leaf streak disease (black Sigatoka) from tion), possibly by increasing the oxygen the Fundacion Hondurena de Investiga- content of the water (Gowen and Edmunds, cion Agricola (FHIA) breeding program, 1973; Sarah, 1993). A final count was made were similarly assessed for putative resis- at 5 days, added to the 2-day count, and the tance to burrowing nematode. These nematode population density adjusted to assessments included 10 FHIA-01 and 10 100 g fresh root weight. Nematodes were ‘Williams’ plants growing in the same field, extracted from the 100-g bulk soil sample and 10 of the recently introduced FHIA-25 using the Baermann tray method (McSor- hybrids growing in monoculture. ley, 1987).
Root Damage Data Analysis After recording the fresh root weight of Nematode population densities and each sample, the percentage of necrotic fresh root weights were log10 (x + 1) trans- roots, hereafter referred to as external formed for analysis. Root damage ratings, necrosis, was estimated. Five primary roots expressed as percentage of necrotic tissue, were then selected from the sample, cut were normalized with a square root trans- into 10-cm-long pieces and split length- formation (Marin et al., 1999; Fogain, wise. The percentage of cortical necrosis 2001). All observations were compared was assessed using a modified scale for bur- with transformed data using Kruskal-Wallis rowing nematode damage (Bridge and ANOVA on ranks, the Tukey test for pair- Gowen, 1993; Speijer and Gold, 1995). wise comparison of means, and Pearson’s This adjusted scale assumed that smaller product moment correlation (SigmaStat, lesions in the outer cortex were caused by SPSS, Inc., Chicago, IL). Nematode popu-
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lation densities on farm #10, containing Helicotylenchus multicinctus, a spiral nema- only spiral nematodes and farm #14, con- tode, was the most prevalent species. It was taining only burrowing nematodes, were found in 15 of the 16 commercial farms evaluated separately for their correlation and together with a small number of H. to root weight and root necrosis. dihystera (Cobb) Sher, averaged more than 23,000 nematodes per 100 g of roots. RESULTS Radopholus similis was also isolated from 15 of 16 farms and averaged 4,680 nematodes Nematode Population Densities per 100 g of roots. Root-knot nematode, Meloidogyne incognita (Kofoid and White) Nematode population densities in roots Chitwood, was recovered from one plant varied widely between commercial farms on each of three commercial farms; galled and among plants within the same farm roots accounted for <5% of each sample. (Fig. 1). Farms 3, 8, and 13 had signifi- Nematodes collected from non-com- cantly more plant-parasitic nematodes mercial farms included the lesion nema- than farm 9, and farm 3 had more than todes, Pratylenchus loosi Loof, extracted farm 10 (P < 0.05). The average popula- from roots of ‘Pata Samoa’, and P. gibbicau- tion density of all nematode species for the datus Minagawa, from an isolated planting 16 farms was 28,500 per 100 g of roots. of ‘Ducasse’ (Musa ABB, Pisang Awak sub-
Fig. 1. Average population densities of spiral (Helicotylenchus spp.) and burrowing (Radopholus similis) nematodes from16 banana farms on Tutuila, American Samoa. Only spiral nematodes were extracted from farm #10 and bur- rowing nematodes from farm #14.
Plant-parasitic nematodes of banana: Brooks 69
group). Nematode population densities DISCUSSION were 5,400 and 8,800 per 100 g roots, respectively. Meloidogyne incognita caused The presence of spiral and burrowing mild root galling (<5%) on various culti- nematodes in most commercial banana vars including ‘Soa’a’ (Fe’i-type), an farms in American Samoa agreed with unusual banana with an upright bunch. Grandison’s (1996) preliminary survey. The average population densities of Bridge (1988) reported that H. multicinctus burrowing nematode on FHIA-01 and ‘Wil- was the most common banana root-para- liams’ growing in the same field were 107 sitic nematode in the Pacific Islands, espe- and 6,353 per 100 g of roots, respectively. cially in the absence of the burrowing The population density of spiral nema- nematode. When both are present in an todes was 31,492 per 100 g of roots on area, it is common to find them together FHIA-01 and 32,130 per 100 g of roots on (McSorley and Parrado, 1986), as in this ‘Williams’. From ten plants of FHIA-25 on study. The lesion nematode, Pratylenchus previously fallowed land, 177 spiral nema- spp., was absent from all commercial plant- todes and 76 burrowing nematodes were ings of the Cavendish-type ‘Williams’. Both recovered per 100 g of roots. Nematode P. loosi and P. gibbicaudatus, recovered from populations in the soil averaged 270 per roots of AAB and ABB Musa genotypes, 100 g of soil and were positively correlated respectively, are new identifications for (r = 0.67, P < 0.005) with root population American Samoa. Pratylenchus loosi, com- densities in the commercial fields. monly associated with damage to tea and coffee (Campos et al., 1990), was extracted Root Damage from roots of ‘Paka Samoa’. This is the sec- ond account of P. gibbicaudatus in the Average fresh root weight per sample South Pacific and only the second con- for the 16 farms was 133 g (57-268 g). firmed isolation from Musa spp. world- There was no correlation between root wide. Pratylenchus gibbicaudatus causes a weight and nematode population density, reddish-black cortical necrosis typical of but there was a negative correlation lesion nematodes and was first reported in between root weight and external root this area from the Cook Islands on banana, necrosis (r = -0.43, P < 0.001), and a weak coffee, and eggplant (Solanum melongena) negative correlation between root weight (Grandison, 1990). and cortical necrosis (r = -0.22, P < 0.01). Population densities of spiral nematode Root necrosis ratings for all nematode were five times greater on average than species averaged 26% (6-62%) for the population densities of burrowing nema- commercial fields, but nematode popula- tode (Fig. 1). The superficial cortical tion density was correlated only with corti- lesions caused by spiral nematodes are con- cal necrosis (r = 0.36, P < 0.0001). On farm sidered less severe than burrowing nema- #10, with just spiral nematodes present, tode lesions, but they are potential entry there was no correlation between popula- points for other soilborne pathogens or tion density and root weight or external saprophytes that can increase root damage. necrosis ratings. Conversely, on farm #14, Few studies have presented data on consisting of burrowing nematodes, popu- both burrowing and spiral nematode pop- lation density was strongly correlated with ulation densities and differing methods cortical necrosis ratings (r = 0.71, P < make comparisons with this study difficult. 0.02), but not with external necrosis. For example, Speijer and Gold (1995)
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extracted 6,037 spiral nematodes and Positive correlations between nematode 2,968 burrowing nematodes per 100 g of population densities and root necrosis were roots after 16-20 hours incubation, and lower than expected. This may have been Speijer and Ssango (1999) reported an due in part to inclusion of necrotic roots in average of 8,935 spiral nematodes and sample estimates and extractions (Price and 10,317 burrowing nematodes per 100 g of McLaren, 1995). Since the nematodes roots following a 24-hour extraction. recovered in this survey are all obligate par- Marin et al. (2000) recorded only burrow- asites requiring living tissue, roots with a ing nematodes and after 7 days estimated higher percentage of necrosis should have 24,745 per 100 g of roots. fewer nematodes than roots with less necro- Variability in nematode population den- sis (Mateille, 1992; Bridge and Gowen, sities among and within farms on Tutuila 1993). To avoid “false-positives”, Price and agreed with a report by Fogain (2001). His McLaren (1995) suggest discarding severely estimated numbers in Cameroon ranged damaged roots from samples before nema- from 5,000 to 150,000 burrowing nema- tode extraction. For example, Speijer and todes per 100 g of roots on farms located in Ssango (1999) estimated the number of the center of the country, and from 800 to dead and functional roots in samples of 172,000 lesion nematodes (Pratylenchus seven Musa cultivars, but estimated cortical goodeyi) per 100 g of roots in the highlands. necrosis and extracted nematodes only Such variation in population densities is from functional roots. In their study, the common under field conditions. This varia- percentage of dead roots (= external necro- tion is due to an aggregated (contagious) sis) and necrotic roots (= cortical necrosis) nematode distribution and the influence of vs. population densities of spiral and bur- factors such as soil heterogeneity, root sta- rowing nematodes were strongly correlated tus, interactions with other organisms, and (r = 0.84 to 0.94, P < 0.001). intra- and interspecific nematode competi- Marin et al. (1998) tested FHIA-01 and tion (Barker et al., 1985; McSorley and Par- FHIA-21 hybrids, both derived from the rado, 1986; Gowen and Queneherve, 1990; burrowing nematode resistant parent SH- Queneherve, 1993; Bridge and Gowen, 3142 (Rowe and Rosales, 2000), against a 1993; Price and McLaren, 1995; Marin et susceptible control (‘Grande Naine’, Musa al., 1998). Seasonal variations in tempera- AAA, Cavendish subgroup) and found no ture and precipitation (McSorley and Par- statistical difference. In this study, FHIA-01 rado, 1986) probably had a minimal effect had 60 times fewer burrowing nematodes on nematode population density. In this cli- than ‘Williams’ growing in the same field; mate soil temperatures are relatively con- the spiral nematode population densities stant and soils drain rapidly (Soil were similar. The newly introduced FHIA- Conservation Service, 1984). However, shal- 25, however, had the lowest nematode pop- low soil, poor drainage, or high water tables ulation densities of any variety tested. may have affected the nematode popula- Based on results from this study, both FHIA tions in small areas of some fields. Differ- hybrids are promising sources of germ- ences in cultivar susceptibility (Speijer and plasm for resistance to the burrowing nem- Gold, 1995) were not a factor in our survey atode in American Samoa. of commercial farms, but variability in ag- Damage thresholds are difficult to gressiveness among nematode isolates apply to bananas because of the numerous needs to be considered (Fallas et al., 1995; factors affecting nematode populations on Marin et al., 1999, 2000). a perennial crop (Gowen, 1995). Reported
Plant-parasitic nematodes of banana: Brooks 71
thresholds vary from 1,000 burrowing nem- AAA cv. Valery) in relation to plant height, dis- atodes per 100 g of roots in W. Africa, to tance from the pseudostem and soil depth. 20,000 per 100 g of roots in Costa Rica Nematology 1:711-716. BARKER, K. R., D. P. SCHMITT, and J. P. NOE. 1985. (Gowen and Queneherve, 1990). Taking Role of sampling for crop-loss assessment and this disparity into consideration, Gowen nematode management. Agriculture, Ecosys- and Queneherve (1990) proposed that tems and Environment 12:355-369. crop losses will occur at nematode popula- BRIDGE, J. 1988. Plant-parasitic nematode problems tion densities greater than 2,000 per 100 g in the Pacific Islands. Journal of Nematology 20:173-183. of roots. This level was surpassed on all BRIDGE, J., and R. GOWEN. 1993. Visual assessment banana farms in American Samoa. Consid- of plant parasitic nematode and weevil damage ering the amount of root damage that was on bananas and plantain. Pp. 147-154 in C. S. associated with these populations, the need Gold and B. Gemmill, eds. Biological and Inte- for nematode management is clearly indi- grated Control of Highland Banana and Plan- tain Pests and Diseases, Cotonou, Benin, Africa. cated. Management options for American CAMPOS, V. P., P. SIVAPALAN, and N. C. GNAN- Samoa include propping of fruiting plants APRAGASAM. 1990. Nematode parasites of cof- to prevent toppling, and ratoon manage- fee, cocoa and tea. Pp. 387-430 in M. Luc, R. A. ment, mulches, and fertilization to increase Sikora, and J. Bridge, eds. Plant Parasitic Nema- plant vigor and root production (Gowen, todes in Subtropical and Tropical Agriculture. CAB International, Wallingford, UK. 1995; Whitehead, 1998). Exclusion is the DANIELLS, J. 1995. Illustrated guide to the identifica- best means of nematode control and dis- tion of banana varieties in the South Pacific, ease-free tissue culture plantlets are the Monograph No. 33. Australian Centre for Interna- first choice for establishing new plantings. tional Agricultural Research, Canberra, Australia. This study confirmed the presence of DAVIDE, R. G. 1995. Overview of nematodes as a lim- iting factor in Musa production. Pp. 27-31 in spiral and burrowing nematodes at levels E. A. Frison, J.-P. Horry, and D. DeWaele, eds. high enough to affect yield. The identifica- New Frontiers in Resistance Breeding for Nema- tion of two lesion nematodes not com- tode, Fusarium and Sigatoka. International Net- monly reported on banana and causing work for the Improvement of Banana and considerable root damage suggests future Plantain, Montpellier, France. FALLAS, G. A., J. L. SARAH, and M. FARGETTE. problems for local growers. This informa- 1995. Reproductive fitness and pathogenicity of tion illustrates the need for continued eight Radopholus similis isolates on banana plants management and scouting efforts. It also (Musa AAA cv. Poyo). Nematropica 25:135-141. provides a baseline for further studies on FIRMAN, I. D. 1975. Plant diseases in the area of the the relationship between nematode popu- South Pacific Commission, 2. American Samoa. South Pacific Commission, Noumea, New Cale- lation densities and yield. donia. FOGAIN, R. 2001. Nematodes and weevil of bananas ACKNOWLEDGMENTS and plantains in Cameroon: occurrence, impor- tance and host susceptibility. International Jour- I am grateful to D. Schmitt, G. Grandi- nal of Pest Management 47:201-205. FOGAIN, R., and S. R. GOWEN. 1997. Damage to son, and B. Sipes for manuscript review, and roots of Musa cultivars by Radopholus similis with to G. Grandison for his support throughout and without protection of nematicides. Nema- the study. This work was funded by USDA tropica 27:27-32. CSREES, Project No. SAM-026. GOWEN, S. R. 1995. Pests. Pp. 382-402 in S. R. Go- wen, ed. Bananas and Plantains. Chapman and Hall, London, UK. LITERATURE CITED GOWEN, S. R., and J. E. EDMUNDS. 1973. An evalua- ARAYA, M., A. VARGAS, and A. CHEVES. 1999. Nem- tion of some simple extraction techniques and atode distribution in roots of banana (Musa the use of hydrogen peroxide for estimating 72 NEMATROPICA Vol. 34, No. 1, 2004
nematode populations in banana roots. Plant NATIONAL AGRICULTURAL STATISTICS SERVICE Disease Reporter 57:678-681. (USDA). 1999. Census of Agriculture_American GOWEN, S., and P. QUENEHERVE. 1990. Nematode Samoa.
Received: Accepted for publication: 16.III.2004 2.IX.2004 Recibido: Aceptado para publicacion: