chapter 16 nematode pests of banana · since root-knot nematodes are present in almost all banana...
TRANSCRIPT
359© Springer International Publishing Switzerland 2017H. Fourie et al. (eds.), Nematology in South Africa: A View from the 21st Century, DOI 10.1007/978-3-319-44210-5_16
Chapter 16Nematode Pests of Banana
Mieke S. Daneel and Dirk De Waele
16.1 Introduction
Banana (Musa) is believed to have originated in the South-East Asian and West Pacific regions where their edible, seed-bearing, diploid ancestors are still found in natural forests. The earliest records dealing with the cultivation of these crops are from India, approximately 2,500 years ago. Although the exact route and time frame of the distribution of Musa outside Asia is uncertain, banana were known during the 15th century on the west coast of Africa, from where the Portuguese introduced them into the Canary Islands. In the 16th century banana were found in Haiti, the Caribbean and tropical America, which is where most export dessert banana are now produced. There are widely varying views on the establishment of banana in East Africa, although it is accepted that they were introduced into Mozambique in the 16th century. Introduction of banana into South Africa (SA) was apparently much later (Jones and Milne 1982).
The banana industry in SA is based on the production of the Cavendish subgroup of cultivars (Musa acuminata Colla; AAA group). The most popular cultivars (cvs) are Grand Nain, Williams, Chinese Cavendish and Dwarf Cavendish (Robinson 1993). Lowland, tropical regions with rainfall in excess of 1250 mm year−1 and minimum temperatures above 15 °C are preferred for banana production (Simmonds 1966). Despite suboptimal conditions with regard to minimum temperatures and rainfall, a banana-growing industry is well established in low-lying and frost-free
M.S. Daneel (*) Agricultural Research Council–Institute for Tropical and Subtropical Crops, Private Bag X11208, Mbombela 1200, South Africae-mail: [email protected]
D. De Waele Laboratory of Tropical Crop Improvement, Department of Biosystems, University of Leuven, Willem de Croylaan 42, 3001 Heverlee, Belgiume-mail: [email protected]
360
areas of SA on an overall area of 11,360 hectares (ha) (DAFF 2011). These regions are Levubu (Limpopo Province), Hazyview and Onderberg (both in Mpumalanga Province), and the North and South Coast of KwaZulu-Natal Province. Lately banana has been grown more extensively in Mozambique in the Maputo and Nampula areas. Swaziland also has a small area under banana.
Plant-parasitic nematodes are a serious problem of banana worldwide (Gowen et al. 2005), including SA. Based on 1996 production figures, Willers (1998) esti-mated that these pests caused a direct loss of 19 % in total production of the crop in SA. Thirty-four plant-parasitic nematode species have been associated with banana in SA (Kleynhans et al. 1996; SAPPNS1). However, economic damage can only be ascribed to a limited number of these species. Plant-parasitic nema-todes usually occur in banana roots or root zones and represent concomitant infestations of three or more species. Quantification of the damage by individual species is, therefore, problematic. Above-ground symptoms of nematode infec-tion on banana can be confused with those associated with damaged or diseased root systems.
The economically important plant-parasitic nematodes associated with banana in SA are root-knot (Meloidogyne spp.), spiral (Helicotylenchus spp.), burrowing (Radopholus similis) (Cobb, 1893) Thorne, 1949, and lesion (Pratylenchus spp.) nematodes. The major species that parasitise banana crops are summarised below with special reference to the symptoms and damage they cause to banana as well as their host range. All nematode pests associated with banana in SA are recorded in Kleynhans et al. (1996), whilst those identified after this publication are being added on a continuous basis to the SAPPNS Database1 (see Chap. 21).
16.2 Root-Knot Nematodes
The root-knot nematode species commonly reported in association with local banana plantations are Meloidogyne incognita (Kofoid and White, 1919) Chitwood, 1949, and Meloidogyne javanica (Treub, 1885) Chitwood, 1949. Meloidogyne are-naria (Neal, 1889) Chitwood, 1949, was found on banana in Zimbabwe (Jones and Milne 1982).
A survey of commercial plantations of banana revealed that root-knot nematodes were present in 93 % of the samples (Table 16.1). Root-knot nematodes were the most abundant and together with spiral nematodes constituted 72 % of the total plant-parasitic nematode complex (De Jager et al. 1999). A similar survey of banana in smallholding plantations in the rural areas of SA and Swaziland showed that root- knot nematodes were present in 93 % of the root samples (Table 16.2) (Daneel et al. 2003).
1 Dr Mariette Marais of the Nematology Unit, Biosystematics Division, Agricultural Research Council–Plant Protection Research Institute is thanked for the use of data from the South African Plant-Parasitic Nematode Survey (SAPPNS) database; E-mail: [email protected].
M.S. Daneel and D. De Waele
361
Table 16.1 Mean number of nematodes recorded from soil and roots in a survey of plantations within the three major commercial banana-producing areas of South Africa (Daneel et al. 2015)
Areaa
Soil samples (250 ml) Root samples (30 g)
Percentage occurrenceOa Hb
S KZNc O H
S KZN
Number of samples 163 124 117 166 119 117Helicotylenchus spp. 474 1142 1953 1059 1292 1532 95Meloidogyne spp. 730 749 835 1571 571 750 93Pratylenchus coffeae 17 55 15 37 76 26 26Radopholus similis 3 14 11 79 45 41 19Paratylenchus sp. (84 %)d 0 0 185 0 0 266 22Rotylenchulus spp. 279 1 0 7 0 0 2Nanidorus spp. 3 31 30 0 0 0 4
aO = OnderbergbH = HazyviewcS = KZN South Coast of KwaZulu-NataldPercentage for KZN as this genus was not recorded from banana in any of the other areas
Table 16.2 Percentage frequency of occurrence of plant-parasitic nematodes associated with banana grown in informal gardens in South Africa and Swaziland (Daneel et al. 2003)
Nematode genera/species
Soil Roots
Locationscna
Percentage occurrenceb n
Percentage occurrence
Meloidogyne spp. 152 96.8 147 93.6 All regionsHelicotylenchus spp. 152 96.8 147 93.6 All regionsRadopholus similis 0
06
3.8 1112
8.9 BBRKN KZN
Pratylenchus coffeae 5025
7.6 0113
3.2 BBRVSEC, S KZN
Rotylenchulus spp. 412
4.4 002
1.3 KSBBR
Nanidorus/Paratrichodorus spp. 11 7.0 – – EC, S KZNCriconemoides spp. 4
32
5.7 – – KN KZNEC, S KZN
Paratylenchus spp. 1 0.6 – – EC, S KZNan number of localities where nematode species were found out of 157 sampledbPercentage of localities where nematodes were present in soil or root samplescLocalities where nematode taxa were present: BBR = Bushbuck Ridge (n = 29); EC and S KZN = Eastern Cape and South KwaZulu-Natal (n = 39); K = Komatipoort (n = 18); N KZN = North KwaZulu- Natal (n = 29); S = Swaziland (n = 7); V = Venda (n = 35)
16 Nematode Pests of Banana
362
16.2.1 Damage
Heavily infected plants are stunted and have thin pseudostems, whilst leaves are yellowish or show discoloured, greenish-yellow bands along the leaf blades (Milne and Kuhne 1968). Infected plants are also prone to wilting during moderately hot days.
Rabie (1991) reported that the concomitant occurrence of root-knot nematodes and various stress factors, including drought and cold temperatures, are involved in inflicting symptoms of ‘False Panama Disease’, which resembles ‘Panama Disease’. In the former case transverse sections of rhizomes of infected plants showed reddish- brown to brownish-purple discoloured vascular tissue. Leaf symptoms include pro-gressive dying back of older leaves, starting at the tips. Galls occur on the primary and secondary roots, whilst distortion of roots and sometimes bifurcation occurs after heavy nematode infections.
Since root-knot nematodes are present in almost all banana plantations (Daneel et al. 2015) (Tables 16.1 and 16.2), it is particularly important to monitor their popu-lation levels in young crops. The general perception is that these nematode pests can cause severe damage to young plants, resulting in suboptimal growth and yield.
16.2.2 Host Range
In the subtropical areas of SA, the host range of both M. incognita and M. javanica includes most broadleaf weed species and cultivated crops. Special attention should, therefore, be given to weeding during fallowing or crop selection for rotation to control root-knot nematodes in banana (Willers et al. 2001).
16.3 Hoplolaimidae
Helicotylenchus multicinctus (Cobb, 1893) Golden, 1956, Helicotylenchus dihys-tera (Cobb, 1893) Sher, 1961, and Helicotylenchus erythrinae (Zimmermann, 1904) Golden, 1956, are the most abundant spiral nematodes that parasitise banana in SA (Jones and Milne 1982; Daneel et al. 2015). A survey of commercial plantations by the latter authors showed that species of Helicotylenchus (mainly H. multicinctus) were present in 95 % of all the samples (Table 16.1). These nematodes had the high-est average numbers overall. Spiral nematodes (mainly H. multicinctus) were also recorded in most of the soil and root samples collected in a survey by Daneel et al. (2003) in the rural areas of SA and Swaziland (Table 16.2). These results agree with those of Gowen et al. (2005), who suggested that H. multicinctus is often the major parasitic nematode on banana where temperature and rainfall conditions are subop-timal for the crop.
M.S. Daneel and D. De Waele
363
16.3.1 Damage
The above-ground symptoms caused by H. multicinctus are similar to those caused by other nematode pests of banana. Toppling may occur when infection levels of this nematode pest are very high (Gowen and Quénéhervé 1990). Symptoms of damage inflicted by H. multicinctus are blackening of the root epidermis, small red-dish lesions in the superficial cortex and a reduction in the number of lateral roots (Jones and Milne 1982). When heavy infections of this spiral nematode occur, lesions coalesce and cause extensive necrosis in the outer root cortex and even root dieback. Lesions may also be present in rhizome tissue of infected plants (Quénéhervé and Cadet 1985). Helicotylenchus multicinctus has no distinct bio-types or races (Gowen and Quénéhervé 2005).
Fig. 16.1 Necrotic areas on a banana root showing damage caused by feeding and migrating bur-rowing nematodes (Kirk West, Port Elizabeth, South Africa)
a b
Fig. 16.2 (a, b) A damaged banana plant infected with burrowing nematodes (a) resulting in top-pling of plants (b) (Kirk West, Port Elizabeth, South Africa)
16 Nematode Pests of Banana
364
16.3.2 Host Range
Most edible banana and plantain cvs and a range of alterative host plants, such as pigweed (Amaranthus spp.), purslane (Portulaca oleracea) and ornamentals (Gowen et al. 2005) are hosts to H. multicinctus.
16.4 Burrowing Nematode
The burrowing nematode, R. similis is a notoriously destructive pest of banana crops throughout the world. However, it is not widespread in SA or in the southern African region. The nematode was present in only 19 % of samples collected during a survey of the three main banana-producing areas, viz. the KwaZulu-Natal Province and Hazyview and Komatipoort (Mpumalanga Province) (Table 16.1) (Daneel et al. 2015). The Levubu and Tzaneen areas in the Limpopo Province are free of R. similis. In a survey conducted in banana in the rural areas of SA and Swaziland, R. similis was found in fewer than 9 % of the root samples examined (Daneel et al. 2003) (Table 16.2). A study on 57 burrowing nematode isolates collected from Australia, Cameroon, Central America, Cuba, Dominican Republic, Florida, Guadeloupe, Hawaii, Nigeria, Honduras, Indonesia, Ivory Coast, Puerto Rico, SA and Uganda showed that 55 of them were morphologically similar to R. similis. Seven of these isolates, all obtained from material collected in Florida (USA), were parasites of citrus (Citrus spp.) (Kaplan et al. 2000). The SA isolates were not para-sitic to citrus, and there is no record that a citrophylic isolate is present in SA.
16.4.1 Damage
Radopholus similis infection causes mass destruction of primary roots and poor anchor-age of banana plants (Fig. 16.1). The nematode could be present throughout the entire root system, including the rhizome (De Villiers et al. 2007). Toppling of plants often occurs during windy conditions when bunches are present, hence the general name of ‘toppling disease’ (Fig. 16.2). Jones and Milne (1982) explained that the lateral move-ment of R. similis in the root cortex, as well as secondary colonisation of the vacated cavities by parasitic and saprophytic fungi, enlarges lesions so that the stele may be disrupted. When this occurs, the entire root beyond the initial nematode entry site becomes functionless. The stele is never entered by this nematode (Jones and Milne 1982).
After the identification of R. similis in SA in 1969 (Jones and Milne 1982), a strict quarantine system was introduced. The practice of using rhizomes as propa-gating material was stopped in SA and many other parts of the world since R. similis could be spread this way. A permit needs to be obtained for the transport of suckers and rhizomes between local production areas. In quarantined regions, notably the KwaZulu-Natal Province, a permit also has to be obtained even to move material
M.S. Daneel and D. De Waele
365
between districts or farms. With the introduction of tissue-cultured propagating material, the spread of this nematode pest between commercial plantations is no longer an issue (Box 16.1 and Figs. 16.3 and 16.4). However, smallholding produc-ers that are still planting suckers need to follow alternative measures to prevent the
Fig. 16.3 Tissue culture banana plants reared in vitro in glass vials in the laboratory (Mieke Daneel, Agricultural Research Council–Institute for Tropical and Subtropcial Crops, Mbombela, South Africa)
Fig. 16.4 Banana plants, derived from in vitro tissue culturing in the laboratory, growing after being transplanted to fields (Mieke Daneel, Agricultural Research Council–Institute for Tropical and Subtropcial Crops, Mbombela, South Africa)
Box. 16.1 Prevention of the spread of Radopholus similis and other plant- parasitic nematodes in and between banana plantationsOriginally banana plantations were developed using rhizomes, which are often infected with plant-parasitic nematodes. Planting such nematode-infected rhi-zomes leads to nematode infections in new plantations. Burrowing nematodes were spread in this way to many banana-growing areas, including SA.
16 Nematode Pests of Banana
366
spread of R. similis (M. Daneel, Agricultural Research Council–Institute for Tropical and Subtropical Crops, Mbombela and D. De Waele, University of Leuven, Leuven, 2016, personal communication).
16.4.2 Host Range
After Duchame and Birchfield (1956) established the existence of a R. similis bio-type that also attacked citrus, it was confirmed that the R. similis that occurs in SA did not attack citrus (Keetch 1972; Milne and Keetch 1976). An experiment was conducted by Keetch (1972) and Milne and Keetch (1976) in which plants were planted in soil infested with R. similis, and the reaction of these plants was noted to determine the host status of these plants. Only 20 out of 100 plants tested were found to be able to act as host for R. similis. However, in both the National Collection of Nematodes (NCN) and South African Plant-Parasitic Nematode Survey (SAPPNS), any record of R. similis in the field is only associated with bananas.
16.5 Lesion Nematodes
The pandemic lesion nematodes are also well represented in the southern African region, but their distribution in banana plantations is limited. Two species of Pratylenchus are regularly found in SA plantations, viz. Pratylenchus coffeae (Zimmerman, 1898) Filipjev and Schuurmans Stekhoven, 1941, and Pratylenchus brachyurus (Godfrey, 1929) Filipjev and Schuurmans Stekhoven, 1941, with the former being more frequently found (Daneel et al. 2003). Pratylenchus coffeae was
Although legislation, developed in SA in 1983, was very effective in limit-ing the spread of R. similis in local banana-growing areas, it was the combina-tion of this legislation with the development of tissue culture plants (as a means of propagating nematode-free plants) that really limited the spread of R. similis. Tissue culture plants are developed in the laboratory from clean planting material and are free of pests and diseases. Before the tissue-cultured plants are distributed to the producers, the plantations have to be tested and declared virus-free.
M.S. Daneel and D. De Waele
367
found in 25.9 % of root and soil samples in commercial plantations (Table 16.1) (Daneel et al. 2015). Samples from several individual plantations had no lesion nematodes, but these pests were widely distributed throughout the banana- producing areas. In commercial banana plantations, lesion nematode numbers varied from 0 to 1,400 nematodes 30 g roots−1. The survey of Daneel et al. (2003) in rural banana- producing areas showed that, although lesion nematodes were present in all areas, P. coffeae constituted only 3.2 % of the nematode pest complex present in banana roots and 7.6 % in soil samples (Table 16.2).
16.5.1 Damage
The symptoms of damage caused by P. coffeae are very similar to those caused by R. similis. They include stunting of the plants, slowing of the vegetative phase, reduction in the number of leaves, lower bunch mass and reduced lifespan of planta-tions. Willers et al. (2001) reported that smallholding banana plantations in the Giyani area (Limpopo Province) were rendered totally unproductive as a result of P. coffeae infections during the crop cycle. This was despite the fact that good man-agement practices were maintained by the producers.
16.5.2 Host Range
Pratylenchus coffeae has a wide host range, including many broadleaf weed species (Gowen et al. 2005). The known host range of P. coffeae in SA is grapevine, banana, citrus and veld (dune thicket, grasses) (Kleynhans et al. 1996 and information from both NCN and SAPPNS databases).
16.6 Reniform Nematodes
The occurrence of Rotylenchulus spp. in bananas has not been studied in detail in SA since it is not regarded as a widespread pest in the banana industry. Rotylenchulus spp. individuals were present in 2 % of the samples in a survey conducted in commercial banana plantations (Table 16.1). Reniform nematodes were only found in the Onderberg area (Mpumalanga Province) in numbers ranging from 0 to 2,985 250 ml soil−1 (Table 16.2).
16 Nematode Pests of Banana
368
16.7 Other
Numerous other nematode species have been associated with banana but are not considered economically important. In a survey of 52 farms, Jones (1979) recorded Nanidorus renifer Siddiqi, 1974, in 53 % of samples, Paratylenchus sp. in 35 %, Scutellonema brachyurus (Steiner 1938) Andrássy, 1958, and Scutellonema trunca-tum Sher, 1964, in 8 %, Tylenchorhynchus ventrosignatus Tobar Jiménez, 1969, in 7 %, Hemicycliophora in 2 % and Xiphinema in 1 %. The survey that was done in commercial banana plantations by the ARC – ITSC showed that Paratylenchus was present only in the KwaZulu-Natal Province where it occurred in 84 % of the sam-ples. Nanidorus/Paratrichodorus spp. were found in only 4 % of all the samples.
16.8 Management Strategies
16.8.1 Legislation
Following the discovery of R. similis in SA, legislation was passed to prevent fur-ther distribution of the pest. The Agricultural Pest Act 36 of 1983 (NDA 2015) requires that a permit must be obtained for the transportation of plant propagation material between individual farms as well as between magisterial districts. The act specifies traditional propagation material such as suckers, rhizomes and setts. Although tissue cultured plants are exempted by the legislation, a permit is also required once they have been established in a nursery.
16.8.2 Preparation of Plant Material
Almost all commercial banana crops are established exclusively from tissue cul-ture material that is free of plant-parasitic nematodes. However, suckers and rhi-zomes are still used to establish new plantings in rural areas, particularly when a shortage of tissue culture material exists. These suckers are infected with plant-parasitic nematodes present in the soil where such planting material was sourced. Paring, to remove visible lesions caused by nematode pests and banana weevil so that only white rhizome tissue remains, is recommended in such cases. In many African countries the rhizome is dipped in hot water for a specific period of time to kill remaining nematode pests, but in SA this technique is seldom or never used. Once cleaned of nematode-infected material, the rhizomes must be planted in soil where nematode pest numbers have been substantially reduced. This could be obtained by using one or combinations of the following strategies (see also Sect. 16.8.3), viz. planting in virgin soil, leaving soil fallow for an extended
M.S. Daneel and D. De Waele
369
period, addition of organic amendments or heat sterilisation using a transparent plastic cover for several weeks. The latter technique can only be done when plant-ing is done in a very small area.
16.8.3 Cultural Control
Fallowing for at least 6 months (Loos 1961; Tarjan 1961) and rotation with selected cover crops can reduce populations of certain nematodes prior to planting banana. Milne and Keetch (1976) tested several cover crops and reported that radish (Raphanus sativus) and Tagetes patula reduced populations of R. similis after 5 months to a level comparable to that of ethylene dibromide (EDB) fumigation. Rotation with Buffalo grass (Megathyrsus maximus var. trichoglum; syn Panicum maximum) and purple bean (Phaseolus atropurpureus) supported neither R. similis nor Meloidogyne spp., whilst growing sugarcane (Saccharum hybrid) eliminated R. similis after 10 weeks (De Villiers et al. 2007). Intercropping with crops such as coffee (Coffea arabica), vegetables, maize (Zea mays) and cassava (Manihot escu-lenta) often used in West and East Africa is not practiced in SA.
Chicken and cattle manure amendments at high volumes (40 MT ha−1 or more) in combination with chemical fertilisers are frequently used in banana produc-tion in SA to suppress nematode pest populations over the long term. Before planting banana, application of 15 MT chicken manure ha−1 or 30 MT cattle manure ha−1 is generally recommended (De Villiers et al. 2007). Stirling (1991) reported that the effect of organic amendments is a complex process that enhances plant growth by improving soil structure and fertility, enhanced plant resistance and the stimulation of micro-organisms, which act as natural enemies of nema-todes. Microbial degradation of organic amendments affects the release of metabolites that have direct nematicidal effects (Stirling 1991). In cases of severe nematode infections, treatment of banana plants with a nematicide is recom-mended (see Sect. 16.8.5).
16.8.4 Biological Control
Daneel et al. (1998) demonstrated the efficacy of the soil fungus Purpureocillium lilacinum (syn Paecilomyces lilacinus) for the control of banana nematode pests including R. similis and Meloidogyne spp. Aside from reducing numbers of nema-todes, the product shortened the period from flowering to harvest of banana. The product was registered for use in SA on banana at a dosage rate of 2 × 109 spores g−1 in suspension at a rate of 2–4 g mat−1, depending on severity of nematode infestation (Van Zyl 2013).
16 Nematode Pests of Banana
370
16.8.5 Chemical Control
Conventional, synthetically derived nematicides have been widely used in SA for nematode control on banana. Although fumigants have been shown to be effective (Keetch et al. 1976), such products are not used in banana production mainly due to high input costs. Pre- and post-plant carbamate and organophosphate nematicide applications are more regularly used for nematode control in banana. These prod-ucts are applied as granular or liquid formulations around the base of the pseud-ostems or suckers. Furfuraldehyde is also registered on banana in SA and can be used when nematode population pressure is not severe (Van Zyl 2013).
In the local banana industry, plant-parasitic nematodes are seldom regarded as the primary yield-limiting factor. Therefore, it is recommended that nematode sam-ples are taken annually and that nematicides are only applied to reduce nematode- pest populations likely to limit yield or cause long-term yield decline.
16.9 Conclusions
Although plant-parasitic nematodes are not the major limiting factor in banana pro-duction in SA, they can still cause severe damage to the crop and reduce yields considerably. Because tissue culture material is used in more than 90 % of the plan-tations replanted, nematode pests seldom become problematic during the first years after establishment of commercial plantations. Besides, many producers send in soil and root samples annually for nematode analysis to monitor plant-parasitic nema-tode populations and follow recommendations. This way, the effect of nematode pests in commercial banana production is effectively limited. However, there will always be a need to investigate alternative strategies to keep nematodes under con-trol. For SA and surrounding countries, the need for nematode management strate-gies in the smallholding farming sector is significant and requires more attention.
References
DAFF (2011) A profile of the South African banana market value chain. Department of Agriculture, Fisheries and Forestry, Pretoria. www.nda.agric.za/docs/AMCP/Bananamvcp2011–12
Daneel MS, De Jager K, Dreyer S et al (1998) PL Plus is an environmentally friendly nematicide for banana nematodes. Neltropica Bull 300:32–34
Daneel MS, De Jager K, Van den Bergh I et al (2015) Occurrence and pathogenicity of plant- parasitic nematodes on commonly grown banana cultivars in South Africa. Nematropica 45:118–127
Daneel MS, Dillen N, Husselman J et al (2003) Results of a survey on nematodes of Musa in household gardens in South Africa and Swaziland. InfoMusa 12:8–11
M.S. Daneel and D. De Waele
371
De Jager K, Daneel MS, Desmet M et al (1999) Pathogenicity and distribution studies to determine threshold levels for nematodes on banana. Banana Grow Assoc S Afr Yearb 3:72–77
De Villiers EA, Daneel MS, Schoeman PS (2007) Pests. In: Robinson JC, De Villiers EA (eds) The cultivation of banana. Ingwe Print, Nelspruit, pp 194–219
Duchame EP, Birchfield W (1956) Physiologic races of the burrowing nematode. Phytopathol 46:615–616
Gowen S, Quénéhervé P (2005) Nematode parasites of bananas and plantains. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford, pp 611–643
Jones RK (1979) Nematodes associated with bananas in South Africa. Phytophylactica 11:79–81Jones RK, Milne DL (1982) Nematode pests of bananas. In: Keetch DP, Heyns J (eds) Nematology
in southern Africa. Science Bulletin No. 400. Department of Agriculture and Fisheries, Pretoria, pp 30–37
Kaplan DT, Thomas WK, Frisse LM et al (2000) Phylogenetic analysis of geographically diverse Radopholus similis via rDNA sequence reveals a monomorphic motif. J Nematol 32:134–142
Keetch DP (1972) Some host plants of the burrowing eelworm, Radopholus similis (Cobb) in Natal. Phytophylactica 4:51–58
Keetch DP, Reynolds RE, Mitchell JA (1976) An evaluation of pre- and post–plant nematicides for the control of plant parasitic nematodes on bananas. Citrus Subtrop Fruit J 506:5–7
Kleynhans KPN, Van den Berg E, Swart A et al (1996) Plant nematodes in South Africa. Plant Protection Research Institute Handbook No 8. Agricultural Research Council–Plant Protection Research Institute, Pretoria
Loos CA (1961) Eradication of the burrowing nematode, Radopholus similis, from bananas. Plant Dis Rep 45:457–461
Milne DL, Keetch DP (1976) Some observations on the host plant relationships of Radopholus similis in Natal. Nematropica 6:13–17
Milne DL, Kuhne FA (1968) Nematodes attack bananas. Farming S Afr 44:5–9NDA (2015) http://www.nda.agric.za/docs/NPPOZA/Agricultural%20Pests%20Act.pdf. Accessed
12 Sep 2013Quénéhervé P, Cadet P (1985) Localisation des nematodes dans les rhizomes du bananier cv Poyo.
Rev Nématol 8:3–8Rabie EC (1991) Die invloed van Meloidogyne javanica en M. incognita op die voorkoms van
Valspanamasiekte by piesangs. MSc Dissertation, University of Pretoria, PretoriaRobinson JC (1993) Handbook of banana growing in South Africa. Dynamic Ad, NelspruitSimmonds NW (1966) Bananas, 2nd edn. Longmans, LondonStirling GR (1991) Biological control of plant parasitic nematodes. Progress, problems and pros-
pects. CAB International, WallingfordTarjan AC (1961) Longevity of Radopholus similis (Cobb) in host free soil. Nematologica
6:170–175Willers P (1998) Nematologiese navorsing in subtropiese bedrywe. Neltropica Bull 299:12–13Willers P, Daneel MS, De Jager K (2001) Banana. In: Van den Berg MA, De Villiers EA, Joubert
PH (eds) Pest and beneficial arthropods of tropical and non-citrus subtropical crops in South Africa. Agricultural Research Council–Institute for Tropical and Subtropical Crops, Nelspruit, pp 34–43
Van Zyl K (2013) A guide to crop pest management in South Africa. A compendium of acaricides, insecticides, nematicides, molluscicides, avicides and rodenticides. A CropLife Compendium, 1st edn. VR Print, Pinetown
16 Nematode Pests of Banana