Microcyclus ulei (South American leaf blight of rubber)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Natural enemies
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Seedborne Aspects
- Plant Trade
- Wood Packaging
- Impact Summary
- Environmental Impact
- Social Impact
- Detection and Inspection
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Microcyclus ulei (Henn.) Arx
Preferred Common Name
- South American leaf blight of rubber
Other Scientific Names
- ?Passalora heveae Massee, nom. nud.
- Aposphaeria ulei Henn.
- Dothidella ulei Henn.
- Fusicladium heveae K. Schub. & U. Braun
- Fusicladium macrosporum J. Küyper, homonym (non F. macrosporium Bonord.)
- Melanopsammopsis ulei (Henn.) Stahel
International Common Names
- Spanish: enfermedad sudamericana de hoja del cauchero
- French: flétrissure sudamericaine des feuilles de l'hévéa; maladie des feuilles sud américaine
Local Common Names
- Brazil: mal das folhas
- Germany: südamerikanischen battfallkrankheit
- Indonesia: Amerika selatan
- Netherlands: zuid-amerikaanse bladziekte
- MICCUL (Microcyclus ulei)
Summary of InvasivenessTop of page The invasive potential of the disease has been illustrated by the devastating impact that it has had on attempts to develop rubber production in South America. Rapid epidemic development of the disease under humid conditions can destroy young rubber plants. Control methods are expensive and reduce the economic value of the crop. The disease poses a major threat to the large rubber producing areas in West Africa and South-East Asia, where strict quarantine measures are enforced to prevent entry of the pathogen (Jayasinghe, 1998).
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Ascomycota
- Subphylum: Pezizomycotina
- Class: Dothideomycetes
- Subclass: Dothideomycetidae
- Order: Capnodiales
- Family: Mycosphaerellaceae
- Genus: Microcyclus
- Species: Microcyclus ulei
Notes on Taxonomy and NomenclatureTop of page South American leaf blight was first mentioned by Hennings (1904), who briefly described the pathogen. He examined infected leaves from native rubber trees collected by Ernst Heinrich Ule at the Juruá River, Brazil in 1901 and near Iquitos, Peru in 1902 (Wellman, 1972). The teleomorph was named Dothidella ulei. The pycnidial anamorph is Aposphaeria ulei. In 1911, Küyper described the conidial anamorph as Fusicladium macrosporum (Rands, 1924).
Following the studies of Hennings and Küyper, Massee, in 1913, described the conidial form as Passalora heveae. Cayla in 1913 and Petch in 1914 concluded that D. ulei, A. ulei and F. macrosporum were forms of the same pathogen (Holliday, 1970). Stahel in 1917 transferred the name from Dothidella to Melanopsammopsis (Rands, 1924). In 1962, Müller and Arx transferred the name to the genus Microcyclus (Holliday, 1970).
Currently, the teleomorph is named Microcyclus ulei (Henn.) Arx, the conidial anamorph is Fusicladium heveae K. Schub. & U. Braun (in Crous and Braun, 2003) and the pycnidial anamorph is Aposphaeria ulei Henn.
DescriptionTop of page The hyphomycetous anamorphic form of M. ulei is characterized by simple, erect or denticulate conidiophores 140 x 4-7 µm, with one to four conidial scars. The conidia are of polyblastic origin, hyaline to slightly brown, with smooth or verrucose external wall, truncate base, 1-septate and 23-63 x 5-10 µm or non-septate and 15-43 x 5-9 µm (Holliday, 1980).
The coelomycetous anamorphic form is characterized by pycnidial conidiomata in the black, exoepidermal, carbonaceous stromata on the leaf surface. The conidiomata are ostiolate, 120-160 µm diameter, with simple or ramified conidiophores, which produce conidia in a phialidic-enteroblastic manner (Sutton, 1980). The conidia are 12-20 x 2-3 µm, cylindrical with dilated ends.
The teleomorphic form has perithecial ascomata which are 200- 500 µm diameter. They are produced in the inner part of the exoepidermal black stromata. The stromata are black, carbonaceous, with a rugose external wall. The inner diameter of the stromatal cavities is 100-200 µm. The asci are 50-80 x 12-16 µm, fissitunicate, clavate and contain eight ascospores. The ascospores are 12-20 x 2-5 µm, hyaline, ellipsoid and fusiform, bicellular, with a slight constriction at the septum (Holliday, 1980).
DistributionTop of page
M. ulei occurs in all original habitats of species of Hevea. It has been found at 15° North in El Palmar, Mexico (Martin, 1948) as well as near 25° South in the state of Paraná, Brazil (Gasparotto et al., 1990). It is important to emphasize that the pathogen does not occur in Asia and Africa, which account for about 99% of the worldwide production of natural rubber.
M. ulei can be classed as invasive within its native range because of its destructive capacity in rubber plantations in the area.
Distribution TableTop of page
The 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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Singapore||Absent, no pest record||EPPO, 2014; IPPC, 2015|
|Mexico||Restricted distribution||Native||Invasive||Martin, 1948; CMI, 1990; EPPO, 2014|
Central America and Caribbean
|Belize||Present||Native||Invasive||CMI, 1990; EPPO, 2014|
|Costa Rica||Present||Native||Invasive||Stevenson, 1935; CMI, 1990; EPPO, 2014|
|El Salvador||Present||Native||Invasive||CMI, 1990; EPPO, 2014|
|Guatemala||Present||Native||Invasive||Rands and Polhamus, 1955; CMI, 1990; EPPO, 2014|
|Haiti||Present||Introduced||Invasive||Compagnon, 1976; CMI, 1990; EPPO, 2014|
|Honduras||Present||Native||Invasive||Waite and Dunlap, 1952; CMI, 1990; EPPO, 2014|
|Nicaragua||Present||Native||Invasive||Langford, 1953; CMI, 1990; EPPO, 2014|
|Panama||Present||Native||Invasive||Holliday, 1970; CMI, 1990; EPPO, 2014|
|Trinidad and Tobago||Present||Native||Invasive||Lamont et al., 1917; CMI, 1990; EPPO, 2014|
|Bolivia||Present||Native||Invasive||Alandia and Bell, 1957; CMI, 1990; EPPO, 2014|
|Brazil||Restricted distribution||EPPO, 2014|
|-Bahia||Present||Native||Invasive||Batista, 1947; CMI, 1990; EPPO, 2014|
|-Espirito Santo||Widespread||Native||Invasive||Gasparotto et al., 1990|
|-Goias||Widespread||Native||Invasive||Gasparotto et al., 1990|
|-Maranhao||Widespread||Native||Invasive||Gasparotto et al., 1990|
|-Mato Grosso||Widespread||Native||Invasive||Gasparotto et al., 1990|
|-Mato Grosso do Sul||Widespread||Native||Invasive||Gasparotto et al., 1990|
|-Minas Gerais||Widespread||Native||Invasive||Gasparotto et al., 1990|
|-Para||Widespread||Native||Invasive||Hennings, 1904; CMI, 1990|
|-Parana||Present, few occurrences||Native||Invasive||Gasparotto et al., 1990|
|-Pernambuco||Present||Native||Invasive||Gasparotto et al., 1990|
|-Rio de Janeiro||Widespread||Native||Invasive||Gasparotto et al., 1990|
|-Sao Paulo||Present||Native||Invasive||Cardoso and Rossetti, 1964; CMI, 1990; EPPO, 2014|
|Colombia||Present||Native||Invasive||Sorensen, 1945; CMI, 1990; EPPO, 2014|
|Ecuador||Present||Native||Invasive||Holliday, 1970; CMI, 1990; EPPO, 2014|
|French Guiana||Present||Native||Invasive||CMI, 1990; EPPO, 2014|
|Guyana||Present||Native||Invasive||Bancroft, 1913; CMI, 1990; EPPO, 2014|
|Peru||Present||Native||Invasive||Hennings, 1904; CMI, 1990; EPPO, 2014|
|Suriname||Present||Native||Invasive||Küyper, 1911; CMI, 1990; EPPO, 2014|
|Venezuela||Present||Native||Invasive||Lasser & Rodrigues, 1944; CMI, 1990; EPPO, 2014|
History of Introduction and SpreadTop of page M. ulei has prevented the large-scale commercial cultivation of rubber in South and Central America. Wherever new plantings were established the disease soon became epidemic and caused the collapse of the enterprise. The pathogen is probably native throughout most of the region on indigenous Hevea species, but man may also have aided distribution (Hilton, 1955; Carefoot and Sprott, 1969). Apart from the record in Haiti, there has been no spread outside South and Central America and strict quarantine practices are aimed to exclude it from Asia and Africa.
Risk of IntroductionTop of page RISK CRITERIA CATEGORY
ECONOMIC IMPORTANCE High
DISTRIBUTION Central & South America
SEEDBORNE INCIDENCE Not recorded
SEED TRANSMITTED Not recorded
SEED TREATMENT None
OVERALL RISK High
Notes on phytosanitary risk
A quarantine law has been established for international air travel in Malaysia because the rapid development of direct air flight connections between tropical countries is enhancing the possibility of the spread of M. ulei: passage from South American countries to Malaysia is prohibited. All rubber plants derived from Wickham plants used in South-East Asian and African countries (Compagnon, 1976) have, so far, proved highly susceptible to M. ulei (Chee, 1976c). Therefore, a main aim of Asian and African countries is the development of control methods against this disease.
Hosts/Species AffectedTop of page M. ulei infects Hevea brasiliensis, H. benthamiana, H. camargoana, H. camporum, H. guianensis, H. pauciflora and H. spruceana, and hybrids between these species. In laboratory experiments, young leaves of cassava were also infected and reacted with hypertrophy and leaf distortion (NTV Junqueira, EMBRAPA/CPAA, Brazil and R Lieberei, University of Hamburg, Germany, personal communication, 1988).
Host Plants and Other Plants AffectedTop of page
|Hevea brasiliensis (rubber)||Euphorbiaceae||Main|
Growth StagesTop of page Seedling stage, Vegetative growing stage
SymptomsTop of page The symptoms vary with the age of the infected leaves. In young leaves of susceptible clones up to 10 days of age, 3-4 days after inoculation, slightly discoloured, hypertrophic deformations are visible. 5-6 days after inoculation, greyish to olive-green masses of conidia are present on the lower leaf surface. When infection density is high, these spore-producing lesions coalesce, the leaves turn reddish and premature leaf fall is observed. The petioles, young twigs and young fruits of susceptible clones can also be infected. When conditions are favourable for disease development and in highly susceptible clones, infection and rapid re-infection of young leaflets can cause successive defoliations which lead to dieback of terminal twigs and branches and ultimately to death of young trees.
In young leaves that are older than 12-15 days, the lesions become smaller, only slightly hypertrophic and conidiospore production is low or even absent. In slightly infected young leaves or infected older leaves, no premature leaf fall is induced, instead, on the upper surface of these leaves, black stromatic areas form. The stromata contain pycnidial cavities in which conidia are formed. Later on, the stromatic areas coalesce to form ring-like structures. The leaf tissue within the rings often disintegrates, creating small holes within the rings. In these older parts of the stroma, ascospores are formed in pseudothecia. (See also Gasparotta and Ferreira, 1989.)
List of Symptoms/SignsTop of page
|Fruit / lesions: black or brown|
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Leaves / abnormal leaf fall|
|Leaves / necrotic areas|
|Stems / canker on woody stem|
|Stems / dieback|
|Stems / discoloration of bark|
Biology and EcologyTop of page Transmission
The spores of M. ulei are disseminated by rain or by wind. Wind is a particularly important factor for distribution of spores within a plantation or from one area to another. Dissemination of conidia occurs mainly between 09.00 and 14.00 h, when temperature is high and relative humidity is at its lowest point. Ascospores are disseminated in the night, with a peak between 06.00 and 08.00 h (Holliday, 1969; Chee, 1976b; Rocha and Vasconcellos Filho, 1978). According to Holliday (1970) and Chee (1976a), the ascospores are liberated when leaves containing stromata are wettened and kept in the dark at 13-16°C.
M. ulei infects young leaflets, those up to 12 days old being most susceptible, but thereafter becoming increasingly resistant. Lesions appear about 4-10 days after infection, on which conidia are produced and young diseased leaves are often shed. Severe conidial infections, which cause fall of young leaflets and increase the quantity of conidial inoculum, are known as the 'exploding phase' of the disease. This is the most important phase of the disease and leads to the physiological debilitation of the trees. Older leaflets that become infected do not suffer premature fall and remain on the tree. 30-60 days after infection, they develop black stromata ('sandpaper' symptoms) on which the other asexual, pycnidial phase of the pathogen develops followed by the sexual, ascospore stage. The importance of the pycnidial phase for the pathogen is still unknown. According to Holliday (1970), the pycnidiospores germinate but do not cause any infection.
After they have reached 4 or 5 years of age, rubber trees change their leaves. Ripe diseased leaves with 'sandpaper' symptoms, whether on the ground or still on the plants, provide ascospores as the primary source of inoculum. These are spread by the wind and reach the young leaflets, where they germinate, penetrate and colonize the tissue. Under favourable conditions for the disease, within 5 or 6 days, the infected leaflets reveal lesions covered with conidia that may also be spread by wind or rain. Conidia are thus a secondary source of inoculum. Stromata formation takes 2 months; it then takes 1 month for asci to form and 1 month for them to 'ripen' and to liberate the ascospores. The complete life cycle thus takes 4 or 5 months. The stromatic ascogenous stage persists on mature diseased leaves and provides the survival stage of the fungus.
The occurrence of the sexual phase enables substantial variability within the pathogen populations that has facilitated the development of new pathotypes able to overcome any host resistance that has so far been used to attempt control of the disease. Rivano (1997a) demonstrated the presence of seven virulence factors and 12 physiologic races in a collection of 16 pathogen isolates tested against 10 differential rubber clones.
Young rubber trees (of up to 3 or 4 years) in freshly established plantations, seed gardens and clone gardens, produce new leaves throughout the whole year. Plants that are older than 4-5 years normally change leaves once a year with the onset of the dry season ('wintering'). This leaf change behaviour is highly important for epidemics of M. ulei, because leaves are only susceptible in their growth phase up to 10-15 days. Mature leaves are completely resistant to M. ulei. The defoliation of successive flushes of new leaves severely debilitates the trees, causing dieback with curtailment of latex production; young trees may be killed.
Infections with M. ulei occur when leaves are wet. Estimates of the period of leaf wetness needed for infection vary. Rands (1924) reported that the pathogen needs 10-12 hours of free water on the leaves for infection. Langford (1945) and Hilton (1955) stated that 8 hours of free water are sufficient for successful infection. Kajornchaiyakul et al. (1984) and Gasparotto et al. (1989a) found that at 24°C not more than 6 hours of free water are necessary for infection. Gasparotto and Junqueira (1994) showed that an isolate of the pathogen did not need more than 3 hours of leaf wetness for infection and other isolates could infect within 4 hours. It must be assumed that the different periods needed for the pathogen to infect the leaf are related to the virulence of the isolates.
Various studies reveal that the optimum temperature for germination of spores of M. ulei is about 24°C (Langford, 1945; Holliday, 1970; Chee, 1976a; Kajornchaiyakul et al., 1984; Gasparotto et al., 1989a). Sporulation was totally inhibited at 20°C (Kajornchaiyakul et al., 1984). Gasparotto and Junqueira (1994) found that some isolates of M. ulei are able to infect and produce spores at 16°C, but other isolates do not sporulate at 20°C. These differences seem to reflect physiological differences between isolates from different ecological regions.
In Brazil, Camargo et al. (1967), working in Pindamonangaba (Sao Paulo) and Rocha, and Vasconcellos Filho (1978) in Ituberá (Bahia) reported that relative humidity higher than 95% RH for 10 hours consecutively at least during a period of 12 nights per month provides the best conditions for the occurrence of South American leaf blight. Gasparotto et al. (1989b) analysed climatic data and disease incidence at Ponte Nova (Minas Gerais) and found that the severity of leaf blight is positively correlated to the periods with leaf wetness, with periods of at least 90% RH and above the minimum temperature, and is negatively correlated with periods of 20°C or lower. Camargo (1976) also found that the median temperature lower than 20°C can be used as an indicator for climatic conditions unfavourable to the development of M. ulei.
According to Gasparotto et al. (1989b), there is no significant correlation between the severity of leaf blight and the frequency of rainfall and the total precipitation. Other parameters such as duration and intensity of rainfall must be analysed, because there may be direct and indirect factors, for example, enhancement of relative humidity and reduction of temperature caused by rain, which affect disease development. For example, in the north-east of Trinidad (annual rainfall >2500 mm) the incidence of leaf blight is less severe than in the north-west region with an annual precipitation between 1300 and 2500 mm (Chee, 1979). In Guatemala, the occurrence of leaf blight is much higher in Navajoa (east region, annual precipitation of 2500 mm) than in los Clavellinas (west region, annual precipitation of 3500 mm). According to Holliday (1969), rains with high intensity and especially with long duration remove spores out of the air and wash them from the leaflets.
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
Notes on Natural EnemiesTop of page The mycoparasite Dicyma pulvinata occurs naturally in Brazil, especially in the Amazon region. D. pulvinata grows as a hyperparasite on stromata, conidia and mycelia of M. ulei, but does not in practice reduce the inoculum density in plantations composed of clones that are susceptible to M. ulei.
Means of Movement and DispersalTop of page Natural dispersal of M. ulei occurs through conidia and ascospores dispersed primarily by wind although rainfall assists spore release and daytime showers can lead to large transient increases in spore concentration in the air. Spore production is reduced during dry weather. Wind may disperse spores over large areas and diseased leaf debris containing the ascospore stage may also become airborne and be carried over shorter distances by gusting winds.
Although spores maybe carried incidentally by 'passive' vectors such as animals and man that may come into contact with diseased rubber foliage, this has not been investigated.
The disease has not been recorded as being seedborne, although fruits of the rubber tree can be infected.
Seedborne AspectsTop of page This pathogen has not been shown to be seedborne.
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Flowers/Inflorescences/Cones/Calyx||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Fruits (inc. pods)||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Leaves||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Seedlings/Micropropagated plants||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Stems (above ground)/Shoots/Trunks/Branches||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Plant parts not known to carry the pest in trade/transport|
|Growing medium accompanying plants|
|True seeds (inc. grain)|
Wood PackagingTop of page
|Wood Packaging not known to carry the pest in trade/transport|
|Loose wood packing material|
|Processed or treated wood|
|Solid wood packing material with bark|
|Solid wood packing material without bark|
Impact SummaryTop of page
|Fisheries / aquaculture||None|
ImpactTop of page South American leaf blight has been compared with other diseases of high economic importance, such as coffee rust (Hemileia vastatrix) and potato leaf blight (Phytophthora infestans) (Hilton, 1955).
The main reasons that this disease threatens plantations include the rapid dissemination of spores, the high capacity for destruction and the difficulty in controlling the fungus. Premature leaf fall caused by M. ulei leads to dieback of trees and economic losses. Retardation of growth in seed orchards and in clone gardens reduces the number of rootstocks needed for budding as well as the amount of budwood from defined clones. Severely attacked defoliated seedlings cannot be budded and no buds can be collected from clone-defined plants because the bark is too hard and cannot be removed in the required manner. In adult plantations, successive attacks of M. ulei cause dieback of twigs or even death of the entire plant. Furthermore, attacked plants are easily infected by other pathogens which contribute to the rapid death of trees. Stahel (cited in Rands, 1924) observed that three successive defoliations within 6 months are sufficient to cause the death of trees of 5 to 6 years of age.
In 1913, South American leaf blight caused serious destruction in rubber plantations in Guyana (Bancroft, 1916). In Suriname, one-third of a plantation of 40,000 trees, planted in 1911, was destroyed in 1918; the plantation was abandoned in 1920 and was substituted by coffee, cocoa and other crops (Rogers and Peterson, 1976). In 1923 the rubber plantation in Guyana was also closed (Rands, 1924). In Panamá, Goodyear established a plantation in 1935, but by 1940 it had been destroyed by M. ulei (Holliday, 1970).
In the 1920s, the USA received a concession from the Brazilian government to plant rubber trees in 1,200,000 ha of land at the margins of the Tapajós River, Pará (Gonçalves et al., 1983). Until 1928, the Ford Company planted 3500 ha of rubber in Fordlândia, but by 1933 about 25% of the plantation was dying as a result of the high occurrence of M. ulei. In 1934, the Ford Company transferred its activities from Fordlândia to Belterra, planting 6570 ha with high-yielding Oriental clones. In 1941 and 1942 the occurrence of M. ulei increased significantly when the canopies of the rubber trees closed over, and in 1943 the plantations were destroyed by severe fungal attacks (Gonçalves et al., 1983).
In Bahia (Brazil), rubber cultivation on an commercial scale started in 1952. Until 1970, 25,000 ha were planted with an estimated production of 5000 tons of dry rubber per year. It was planned to enhance the rubber production up to 25,000 tons per year in 1975 (Medeiros and Bahia, 1971), but in 1965 M. ulei caused the first severe damage to established plantations and many plantations were abandoned, especially in the area of Una.
Despite the high disease incidence in the Amazon region, in 1972 a programme was started to enhance rubber tree cultivation in this area. The programme was well accepted and in 1982 about 75,000 ha of rubber plantations were established. As in all previous cases, when the rubber trees developed a closed canopy (around 5 years of age), the trees were severely attacked by South American leaf blight.
The disease has, however, had a positive impact on promoting the development of the rubber industry and subsequent economic development in those parts of the world (Africa and especially Asia) where the disease does not occur.
Environmental ImpactTop of page Destruction of rubber plantations results in changes of land use. Many abandoned areas revert back to secondary forest. The disease itself, being part of the native mycoflora, has had no lasting impact on the natural environment or on biodiversity.
Social ImpactTop of page The disease had substantial social impacts on those involved in developing the rubber industry in South America and followed on from the economic aspects resulting in the loss of employment and migration of labour. See Carefoot and Sprott (1969) for a popular account of the disease and its socio-economic impacts.
DiagnosisTop of page The fungus can be isolated using direct transfer of conidia from highly sporulating lesions of freshly collected young leaves. The conidia are placed on potato-dextrose agar and incubated at 24°C. The resulting colonies are small, globose and grey-greenish. After 10-12 days the first spores are produced. For intensive spore production, fragments of colonies are transferred to an agar (20 g/l) supplemented with 10 g sucrose, 6 g peptone, 2 g KH2PO4, 1 g MgSO4.7H2O and 1 ml of a 15% (g/v) chloramphenicol solution. After sterilization, 10 mg lysin-HCl, 0.25 mg tryptophane and 0.25 mg threonine are added. Fungal growth and heavy sporulation occur after 12 days' growth at 24°C, with three repetitions of 1 hour light (about 2000 lux) interrupted by 3 hours of dark, followed by 15 hours of dark. The light intervals are necessary for maximum spore production. The times may be changed according to the strains in culture (Junqueira et al., 1984). The addition of coconut water to the culture medium greatly increases conidia production (Mattos, 1999).
Detection and InspectionTop of page Disease symptoms are easily visible in the field (see Symptoms).
Prevention and ControlTop of page Introduction
The control of South American leaf blight is extremely difficult, because the plants grow up to 25 m high, the pathogen reveals a high physiological variability and, at present, there are no high-producing clones with satisfactory horizontal resistance. In the humid tropical region of the Amazon there is a chance to establish new rubber plantations using crown budding of high-producing clones with crowns of Hevea species that are resistant to M. ulei.
The most efficient method of control is to use resistant productive clones, but clones with a sufficiently high resistance (race non-specific resistance) and good production have been difficult to find so far. The resistance of new selections is generally broken within a few years by the high variability of the pathogen. For example, Clone IAN 6158 was considered to be resistant up to 1990, but in 1991, after 700 ha had been planted in Amazonas state, the trees were severely attacked and the plantations were abandoned (Gasparotto et al., 1992). Promising clones have recently been selected in Sao Paulo state (de Souza et al., 2000). Rivano (1997b) found that Hevea clones from South America possessed the highest levels of resistance whereas those from Asia were most susceptible. Evaluation of resistance showed that smaller lesion size and lower sporulation were the main components and rates of accumulation of a phytoalexin, scopoletin and lignin were strongly correlated with resistance (Garcia at al., 1999). Quantitative trait loci (QTLs) have been identified in Hevea germplasm which impart resistance to the disease (Lespinasse et al., 2000).
Budding of very productive rubber tree stems with crowns of clones of Hevea species that are resistant to M. ulei is an important control method, especially in areas of high disease incidence such as the Amazon basin. According to Gasparotto et al. (1995), crown budding must be used as a plant management method in the humid Amazon area in order to substitute susceptible crowns totally or at least partially. In these 'mixed-crown' plantations, the plants with resistant crowns will serve as a barrier to the dispersal of inoculum and concurrently represent a favourable environment to natural enemies of both pathogens and phytophagous insects. In 'mixed-crown' plantations, the non-budded plants should consist of clones with a certain level of resistance or tolerance.
In Brazil, at EMBRAPA/CPAA (Manaus, Amazonas), researchers are attempting to identify those combinations of disease-resistant crowns with high-producing stems that reveal the lowest depression of latex production. Such depression in latex production partly results from a low number of latex vessel rings in clones used as crowns. A test system based on the structural anatomical aspect has been developed for Hevea pauciflora plants, which are generally suitable for crown budding (VHF Moraes, EMBRAPA/CPAA, personal communication, 1995). The depression of latex flow can be partially overcome by stimulation with ethephon and the addition of magnesium also enhances latex production. The availability of magnesium in the stem latex vessels seems to be reduced when a H. pauciflora crown is combined with the stem of a high-producing clone (Moraes, 1997).
Establishing plantations in 'escape areas' is used to control Southern American leaf blight. These areas have climatic conditions that are unfavourable to M. ulei but suitable for economic rubber tree growth. In various studies, escape areas have been identified in Brazil, for example in the Açailândia-Maranhao state. The rubber trees have a normal production without being attacked by M. ulei, though its presence is detected in seed gardens (Pinheiro et al., 1982). Plantations on the banks of the large rivers of the Amazon region (Bastos and Diniz, 1980) and in the Sao Paulo highlands (Camargo et al., 1967) are considered to be escape areas. On-shore sea breezes were considered to reduce the occurrence of conditions favourable for the development of the disease near coasts (Pezzopane et al., 1996).
In escape regions it is necessary to search for adapted clones that change their leaves in a very short period and only during conditions which are unfavourable to the pathogen. When leaf fall occurs two times per year or in the 'wrong' weather conditions the disease will be favoured.
In Brazil, rubber plantations cover about 200,000 ha. About 90% of the plantations are located in disease escape areas, especially in the states of Sao Paulo, Mato Grosso and Espírito Santo.
Fungicides used to control M. ulei include benomyl, bitertanol, carbendazim, chlorothalonil, fenarimol, mancozeb, propiconazole, thiophanate-methyl, triadimefon, triadimenol, triforine, fenbuconazole and myclobutanil (Gasparotto et al., 1990; Santos and Pereira, 1991; Furtado et al., 1995). In southern Bahia (Brazil), no satisfactory control level was reached using benomyl, carbendazim or thiophanate-methyl (Santos and Pereira, 1985), probably because of fungicide-resistant strains. The presence of benomyl-resistant M. ulei strains in Bahia had been described by Hashim (1988). Furtado et al. (1995) found that fenbuconazole, mancozeb and triadimefon were most efficient.
In seed gardens, clonal gardens and young developing plantations, terrestrial sprayers, tractor-mounted pneumatic sprayers or atomizers can be used. Chemical control is difficult, however, in productive rubber plantations: the trees are up to 25 m high and conventional spraying equipment does not reach the canopy. Aerial spraying, used in south-east Bahia (Brazil), is extremely expensive and not economically feasible for smallholdings and medium-sized plantations, especially when the plantations are dispersed and at far distances from one another, as found in the Amazon. Thermal fogging, though effective in Malaysia against Glomerella cingulata, Oidium heveae and Phytophthora botryosa (Lim et al., 1978; Lim, 1982), was abandoned in Brazil, due to unsatisfactory results when applied on a commercial scale (Albuquerque et al., 1988). Dusting gave good control in southern Bahia (Pereira, 1993).
The time and equipment used for fungicide application depends on the developmental stage of the plants and the plantations. In seed gardens and clonal gardens in areas of high disease occurrence, spraying must be done weekly in the rainy season and at 2-weekly intervals during the dry season. In adult plantations, spraying must be done during the refoliation period at weekly intervals, until the leaves reach their mature state. It is difficult to reach the canopy using normal spraying equipment.
The effect of various sterilants on the viability of conidia has been studied in relation to the risk of spores being carried in transit on passive vectors (LebaiJuri et al., 1997).
The mitosporic fungus Dicyma pulvinata is found growing on conidia, forming lesions and on stromata of M. ulei. Application of D. pulvinata spores to highly susceptible monoclonal plantations does not lead to disease control in these plantations (Junqueira and Gasparotto, 1991), but the fungus may serve as an important component in systems of integrated control and has been developed for potential commercial use (Bettiol, 1996).
For integrated control measures, additional aspects such as enhancement of resistance by vesicular-arbuscular mycorrhiza have to be taken into account (Feldmann, 1991). In plants that are colonized by mycorrhiza, the incubation period of the leaf pathogen is prolonged, whereas sporulation and lesion diameter are diminished.
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