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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 conidial 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 spermogonial cavities in which spermatia are formed. Later on, the stromatic areas coalesce to form ring-like structures. The leaf tissue within the rings often disintegrates, creating small holes (‘shot-hole’ symptoms) within the rings. In these older parts of the stroma, ascospores are formed in pseudothecia. (See also Gasparotto and Ferreira, 1989; Hora Júnior et al., 2014).
The control of SALB 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 P. ulei. However, it has been concluded recently (ASEAN, 2018; Guyot and Le Guen, 2018) that control measures, including breeding and agronomic practices, have not been successful, thus far: chemical methods proving to be expensive and impractical due to the necessity for repeated applications; and, breeding strategies have been ineffective due to the evolution of new races or pathotypes of P. 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 et al., 1999); especially since scopoletin has been shown to be fungitoxic. Similarly, infected or damaged plants release cyanide (HCN) – cyanogenesis has been identified as an obligate feature of rubber trees – which may also be involved in host resistance (Lieberei, 2007).
Quantitative trait loci (QTLs) have been identified in Hevea germplasm which impart resistance to the disease (Lespinasse et al., 2000; Priyadarshan and Gonçalves, 2003). Thus far, eight QTLs with respect to resistance have been identified on seven linkage groups (Lieberei, 2007), whilst seven microsatellite markers have been characterised opening up the possibility of marker-assisted breeding (Lieberei, 2007).
Budding of very productive rubber tree stems with crowns of clones of Hevea species that are resistant to P. ulei is an important control method, which was developed during the Fordlandia-Belterra era in the 1930-40s (Eidt, 1953; Hilton, 1955; Davis, 1997) 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.
Establishing plantations in 'escape areas or zones' is used to control SALB in the Americas. These areas have climatic conditions that are unfavourable to P. ulei, typically with cooler, less humid climates, but suitable for economic rubber tree growth. In various studies, escape areas have been identified in Brazil, and about 90% of rubber plantations are located in these zones, notably in the states of São Paulo, Mato Grosso and Espírito Santo (Camargo, 1976).
In escape areas 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.
More recently, climatic risk analysis has been used to establish the threat posed to other rubber-producing countries by SALB, as well as to identify potential escape zones (Roy et al., 2017; Golbon et al., 2019).
Due to the variable regulations around (de-)registration of pesticides, we are for the moment not including any specific chemical control recommendations. For further information, we recommend you visit the following resources:
SALB has been compared with other diseases of high economic importance, such as coffee rust (Hemileia vastatrix) and potato leaf blight (Phytophthora infestans) (Hilton, 1955; Agrios, 2005) which have the potential to change the political history of the world (Evans, 2002).
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 P. 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 mature plantations, successive attacks of P. 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 (1917) 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, SALB caused serious destruction in rubber plantations in Guyana (Bancroft, 1916) and led to the abandonment of rubber production in 1923 (Rands, 1924). 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 Panamá, Goodyear established a plantation in 1935, but by 1940 it had been destroyed by P. 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 Fordlandia, but by 1933 about 25% of the plantation was dying as a result of the high occurrence of P. ulei. In 1934, the Ford Company transferred its activities to a nearby better-drained area (Belterra), planting 6570 ha with high-yielding Oriental clones. In 1941 and 1942, the occurrence of P. 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) and the programme was more or less abandoned despite the fact that promising material had been developed, with the top-budding of over 2 million trees using the resistant H. spruceana (Eidt, 1953; Dean, 1987; Davis, 1997).
In Bahia (Brazil), rubber cultivation on a 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 P. 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, and the earlier Ford Company fiasco, 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 SALB (and this Brazilian rubber programme (PROBOR) was stopped in 1986 (Lieberei, 2007).
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.