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Infection of oil palm can occur at any stage of its life-cycle and the stem fractures in severe disease progression (Rees et al., 2012). Young palms usually die within 6-24 months after the first symptoms are observed, whereas mature palms may withstand the infection for another 2-3 years before dying (Paterson, 2007). The first symptoms of infection are similar to drought conditions. Fully elongated but unopened spears are seen in the centre of the crown (Corley and Tinker, 2015). This indicates that the stem or root system is already extensively damaged, thereby restricting water uptake, but this is not diagnostic for basal stem rot. The lower leaves collapse in old palms and they hang downwards vertically from the point of attachment to the trunk and drooping of younger leaves follow which turn a pale olive-green or yellow and die back from the tip. The base of the stem blackens and later, gum may exude and the basidiomata of G. boninense appear. The crown of the palm may then fall off or the trunk collapses. The peripheral tissues are hard and unaffected by rot, with the black fibres in this zone being normal. The majority of the stem tissue is yellow and disintegrates readily within the stem at the base. Mycelium can be found extended through the tissues. Roots are also found infected with the cortex being brown and decaying and the stele black. Large numbers of basidiomata may be formed with the early ones being small and rounded and the later ones being typical basidiomata. Palms normally die within 6 to 12 months after the appearance of unexpanded spear leaves.
Histopathological studies show that the fungus colonized the cortex, endodermis, pericycle, xylem, phloem and pith of the palm (Rees et al., 2009). In older roots, the fungus may be observed as a whitish skin-like layer on the inner surface of the exodermis. As root tissues will be infected before foliar or stem lesion symptoms are observed, they are often found completely dead and colonized by many saprophytic micro-organisms. Once the palm dies, basidiomata frequently appear along the entire trunk, indicative of a more rapid saprophytic colonization of the tissues.
The currently used control strategies for basal stem rot (BSR) include physical, chemical and biological methods. These are intended to (a) curtail the incidence of BSR after replanting and (b) increase the productive life of the infected oil palm. The extent to which they are effective is debatable. Physical control methods depend on accurate diagnostic methods, which are unavailable as mentioned, making control even more problematic. Sanitation involves elimination measures such as clean clearing and windrowing. They intend to minimize the spread of the inoculum although they are expensive. An open burning technique was used but is banned in Malaysia under the Environmental Quality Act (EQA, 1974). The Indonesian government has issued numerous laws on land fires but these are poorly regulated as recent (2019) fires testify. The disease may be reduced by clearing old trees before they reach greatest susceptibility. Infected palm trunks usually take 2 years for complete degradation. However, windrows often harbour pests, such as the Asiatic rhinoceros beetle (Oryctes rhinoceros) and rats, and may allow fungal pathogens to survive (Paterson et al., 2000) and become sources of infection for the healthy palms.
Minimization of wounds to the palm is desirable as G. boninense may infect via this route. Sanderson et al. (2000) discussed the prevention of the formation of basidia (brackets) to control disease. Infected palms were removed from the plantations, the trunk base and root ring were excavated to 10-15 cm below ground, and the area was covered with soil to prevent further bracket formation. In addition, removing basidiomata from diseased palms and painting them with carbolineum (fungicidal paste) (Turner, 1981) to avoid spore dispersion was also suggested.
Controlling BSR by means of surgery by the excision of the diseased part of the outer stem tissues and applying a protectant coating (coal tar or thiram) was used to treat the open surfaces to prevent further decay (Turner, 1981). Paints or fungicide as dressing also can be a potential control. Mixed results occurred in the treated palms, which has led to a decline in the practice. Curative surgery requires frequent repetitions, as infection often re-emerges if the lesions are not completely removed.
In some estates in Sumatra, Indonesia, mounding has become routine practice for all infected palms over 15 years old, prolonging their economic life (Hasan and Turner, 1998). The economic life of G. boninense-infected oil palms are extended by this treatment. Also, weakened boles are supported thus preventing them from being toppled by wind and further to stimulate the formation of new roots (Turner, 1981). Soil mounding appears an effective treatment.
The cost/benefits of treatments require reassessment especially in view of forthcoming climate change when diseases may increase (Paterson 2019a, b). Findings suggest that low molecular weight phenolic compounds can control the disease (Surendran et al., 2018). Fertilizers are also linked to increased climate change by releasing large quantities of nitrous oxide into the atmosphere (Paterson and Lima, 2018). Continuous supplementation of calcium/copper/SA may be key to enhancing disease resistance in oil palm (Rahamah Bivi et al., 2016). More field work is required based on these results.
Biological control agents often suffer from lack of effectiveness in the field due to susceptibility to environmental conditions namely temperature, humidity, soil pH, etc. These have not provided a solution to BSR. A large-scale nursery trial was conducted in Indonesia using more than 25 biological control agents and incidence was significantly lower in palms treated with T. harzianum (Susanto et al., 2005). This treatment was suggested to prolong the life of palms by up to 2-3 years. Theoretically, biocontrol is an advance compared to other approaches and bio-fungicides are available in the market. However, the efficacy of the preparations in the field is a major concern and they have not cured BSR by any means.
It is worth considering the commercial products that are available. Citing them here does not guarantee that they are effective and in fact only one has been reported in an international journal with an acceptable impact factor: Draz-M is an arbuscular mycorrhiza formulation which reportedly prolongs productivity of 25-year-old infected oil palms and increased their oil yield by 42 and 68% (Sariah and Zakaria, 2000). Generally, suitable control systems have still to be found, developed and/or extensively tested in field trials.
Biodegradation of oil palm debris for disease control
Once oil palm has become diseased and fallen over, managing the waste is a major issue. Enhanced biodegradation is a possible method to degrade the waste but requires more work to find a practical procedure (Paterson et al., 2000). White rot hymenomycetes were utilized to antagonize Ganoderma and increase the rate of oil palm debris degradation (Naidu et al., 2017). Strains of Nocardiopsis, Streptomyces violaceorubidus and Streptomyces isolated from empty fruit bunches had enzymatic potential and antagonistic activity against Ganoderma (Ting et al., 2014). However, these are not white rot fungi and will not degrade lignin as effectively as white rot fungi.
Resistant planting materials
Breeding programmes now exploit genetic resources to provide resistance to diseases (Rival and Jaligot, 2010). Genetic resistance was confirmed by Durand-Gasselin et al. (2005). However, the genes for Ganoderma resistance have not been investigated. Tisné et al. (2017) identified Ganoderma resistance loci in oil palm. A transgenic approach is potentially promising but unlikely to provide an immediately commercially acceptable solution.
There are few investigations where control methods have been tested on a large scale in plantations: these are likely the most suitable methods for general application. Sundram et al. (2015) demonstrated that a combination of Glomus intraradices [Rhizophagus intraradices], Glomus clarum [Rhizophagus clarum] and Pseudomonas aeruginosa significantly improved biocontrol and can reduce BSR disease by 80%. However, trials need extension to mature oil palms and not just seedlings. A field trial for Ganoderma control indicated that treatment with T. harzianum and G. viride was superior to Bacillus sp. A large-scale trial showed that the disease incidence was lower in a field treated with the agents than in untreated fields (Susanto et al., 2005). A preparation should be available by now from this work that was proven to control the disease beyond any doubt, but this is not the case. We have entered a new paradigm where all methods require re-evaluation on a cost/benefit basis especially if at least some control was observed in these preliminary studies, because of increased BSR from climate change (Paterson 2019a, b).
Land preparation procedures are based on the largely wrong assumption that infection occurs by mycelial spread from root to root and that the removal of stumps and large pieces of debris will eliminate viable residual inoculum from the field before planting of the next crop. However, removal of debris may be an effective source of basidiospores. Such practices have been widely adopted throughout South-East Asia, to different degrees, dependent on BSR incidence in previous plantings, labour availability and the costs involved. More scientific studies are required to prove its worth.
These methods are based on the concept of root to root infection of the disease which is now considered as less important than basidiospores primary and secondary infection (Pilotti et al., 2018). However, clean clearing will at least remove plant material from further colonization by the fungus hence decreasing basidiospore formation. Current procedures involve excision and removal of all remaining bole fragments by digging pits 1.5 m square and 60 cm deep from both untreated vacant points and diseased palm points. Cauterization by burning of the root-ends along the sides of the pits is also common. In areas with a high incidence of BSR, it is generally thought that all remaining fragments from the previous crop should be brought to the surface for subsequent removal. However, as this is frequently regarded as too costly, and as open burning is now forbidden in Malaysia under the Clean Air Regulations Act of 1978, a common practice is to shred all palm fragments. These can either be scattered over the whole field or stacked in rows and covered with a legume cover crop to facilitate decay and deter colonization of the palm debris from Oryctes. Shredding oil palm tissues has been adopted in some areas in Malaysia but not in Sumatra (Flood et al., 2000).
Darmono (1998) described disease incidence of 51% in some areas of Sumatra, Indonesia. More recent estimation of disease is provided for Malaysia and Sumatra in Paterson (2019, a, b). Basal stem rot (BSR) infection of oil palms in Thailand remains low (Likhitekaraj and Tummakate, 2000): Pornsuriya et al. (2013) indicated that levels were at 1.53%, although they state that the disease was experienced widely in southern plantations. The BSR levels may be influenced by being contiguous with peninsular Malaysia where the disease levels are high (Paterson, 2019b). A scenario of 10% infection currently is a reasonable scenario for Thailand. Papua New Guinea has an important palm oil industry (Corley and Tinker, 2015). The level of BSR in Papua New Guinea is not as high as in some other areas of South-East Asia although 50% has been recorded (Pilotti, 2005; Pilotti et al., 2018). An average of 25% infection is a plausible scenario for this country as the initial level is lower than that used for Malaysia and Sumatra, Indonesia. The Philippines has an oil palm industry at a lower level than that of Thailand (Corley and Tinker, 2015). BSR will be low as the plantations have not been established recently (Woods, 2015) and distances between plantations will be high. Equally, there are no reports of infection by BSR in the literature. Hence a low level of BSR can be expected. BSR of oil palms has been recorded widely throughout the tropics and is considered as a serious disease in Africa and South America.
Infection of young palms has become a serious problem in Papua New Guinea (Pilotti et al., 2018). The malady affects mature oil palms, young palms and seedlings in Malaysia and the fungus can reduce yields by ca. 50-80% (Corley and Tinker, 2015). A 1% disease incidence caused an annual loss of 38 M US$ in Indonesia based on 1996 prices (Darmono, 2000). A 30% increase in BSR between current time until 2070, as may occur in Sumatra, Indonesia (Paterson, 2019a), would cost 1140 US$ under 1996 prices if extrapolated to the whole of Indonesia. G. boninense caused losses of 50 to 350 M US$ per annum in later estimates (Ommelna et al., 2012). The total value of the industry is 50,000 M US$ per annum (Paterson and Lima, 2018) and so the disease represents 0.1 to 0.7% of the total value. The economic loss was estimated recently as $365 million per annum (Seman, 2018). Despite these being small percentage losses compared to the total value of the industry, high disease levels in individual plantations are catastrophic and climate change will have a devastating effect if not ameliorated (Paterson, 2019a, b).Oil palms are frequently monocultures in South-East Asia on areas previously supporting other plantation crops such as rubber or coconuts, or may be planted on areas cleared from primary forest (Paterson and Lima, 2018). Smallholder farmers also grow oil palms in mixed cropping systems with other perennials such as coconuts, coffee and cocoa. Basal stem rot of oil palms is now regarded as the most important disease of oil palms in Malaysia and Indonesia, and can result in stand losses of between 50 and 85% over the 25-year economic life of oil palms. Furthermore, infection tends to occur at a progressively earlier stage in the life of oil palms, and more frequently with each successive planting, such that widespread losses can occur in young plantings of less than 5 years. Cases of BSR can be seen after only 1-2 years in the field when replanting after coconut (Ariffin et al., 2000).
The future effect of the disease under climate change has been assessed by (Paterson, 2019a, b). The infection of oil palm by G. boninense is intimately linked to the health of the oil palm (Paterson et al., 2015, 2017; Paterson and Lima, 2018; Paterson, 2019a, b). Oil palm will be severely affected by climate change with the climate becoming increasingly unsuitable for growth of the palm particularly after 2050 making the palm more susceptible to BSR per se. In addition, G. boninense is liable to become more virulent with climate change corresponding with the increase in disease symptoms since the Second World War (Paterson et al., 2013; Paterson, 2019a, b). Hence the impact of BSR is likely to increase in Sumatra dramatically by 2050 and further until 2100, together with greater difficulty in growing oil palm. Sumatra can be considered as a model for other growing regions in South East Asia (Paterson, 2019a). Paterson (2019b) considered the effect of BSR in Malaysia and also using Agriculture 4.0 methods of modelling and ‘big data’ similar to that in Paterson (2019a) and found that BSR may increase dramatically with large decreases in suitable climate for growing oil palm. The oil palm industry may become unsustainable after 2050. Methods to mitigate the effect of climate change on oil palm production are provided in Paterson and Lima (2018) and work in this field is required urgently. In addition, oil palm growing countries need to support efforts to maintain global warming to the lowest possible increases such as discussed in the Paris climate agreement if the industry is to survive.