S.S. Current 5 Lee Status of Root Diseases of Acacia mangium. Willd. S.S. Lee. Introduction

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1 S.S. Current 5 Lee Status of Root Diseases of Acacia mangium The Current Status of Root Diseases of Acacia mangium Willd. S.S. Lee 5 Forest Research Institute Malaysia, Kepong, Kuala Lumpur, Malaysia Introduction Acacia mangium Willd. is indigenous to the far eastern islands of Indonesia, the Western Province of Papua New Guinea and north-east Queensland, Australia. Its potential for wood production due to its rapid growth was recognized in the 1970s and establishment of large-scale A. mangium plantations in South-East Asia began in the 1980s. Today there is an estimated 600,000 ha of A. mangium, planted mainly in Indonesia, China, Malaysia, the Philippines, Thailand and Vietnam (Kamis Awang, Serdang, 1998, personal communication). A. mangium was first introduced to Malaysia in 1966, where it was planted as firebreaks in Sabah (Yap, 1986). Presently there are approximately 100,000 ha of A. mangium plantations in the country, with approximately 50,000 ha each in the peninsula and Sabah, respectively, and relatively small areas in Sarawak. In earlier reports, A. mangium had not been reported to suffer from any serious diseases (Turnbull, 1986). However, recent studies have shown that tropical acacias, including A. mangium, planted outside their natural range do indeed suffer from a variety of diseases; one of which is root rot (Khamis, 1982; Lee, 1985, 1993; Arentz and Simpson, 1988; Almonicar, 1992). In a survey of A. mangium provenance trials at three locations in Peninsular Malaysia, Lee (1997) found that root-rot diseases were the most frequently occurring diseases, causing between 5 and about 25% mortality of 10-year-old trees. This disease has also been identified as the most significant disease of tropical acacia plantations in Australia, Indonesia, Malaysia, Thailand and India (Old et al., 1997). CAB International Ganoderma Diseases of Perennial Crops (eds J. Flood, P.D. Bridge and M. Holderness) 71

2 72 S.S. Lee Avariety of basidiomycete fungi have been reported to be associated with root rot diseases of A. mangium. Abrown root disease caused by Phellinus has been reported from Sabah (Khamis, 1982) and the Philippines (Almonicar, 1992; Millitante and Manalo, 1999). In the Gogol Valley of Papua New Guinea, Arentz (1986) reported 29% mortality of 5-year-old A. mangium trees due to root disease caused by a species of Ganoderma. Ganoderma spp. are also suspected as the causal agents of root disease of A. mangium trees of various ages in Peninsular Malaysia (Lee, 1985, 1997), Sumatra (Lee, 1997) and West Kalimantan, Indonesia (unpublished data). Here, the results of a long-term survey of root diseases in an A. mangium plantation in Peninsular Malaysia are presented, and preliminary results of pathogenicity tests with the associated fungi are discussed. Impact of Root Diseases on A. mangium Between September 1991 and June 1992 plots were established in an A. mangium plantation in Kemasul, Pahang in Peninsular Malaysia, to monitor the occurrence and spread of root disease. Three replicate plots, each containing rows of trees were set up in stands planted by the Forestry Department in 1982, 1984, 1985, 1986, 1987 and 1988, making a total of 18 plots. All the trees in each plot were numbered and mapped for ease of the survey and future reference. During each survey, symptoms and signs of root disease and the health status of each tree in every plot were recorded. For the first 3 years, surveys were carried out at 6-monthly intervals and thereafter, annually (when it became clear that there were few changes over a 6-month period). Symptoms of root diseases included yellowing, wilting and reduced size of the foliage, thinning of the crown, dieback, and death of trees in groups. Trees with such symptoms were found to occur in patches, with a concentric pattern of spread. Diseased roots were covered by a wrinkled, reddish-brown mycelial skin, encrusted with soil, or encrusted in a mass of earth and sand intermingled with rusty brown patches, in contrast to the clear, pale yellowish-brown coloured healthy roots. More than 40% mortality was observed in all the 1984 plots 14 years after planting, and in plots 1987B, 1988C, 9 and 11 years after planting, respectively (Fig. 5.1a and b). In the 1984 plots mortality increased very rapidly when the trees were between 10 and 14 years old, while in plots 1987B and 1988C, a rapid increase in mortality occurred when the trees were between 6 and 9 years old and 7 and 11 years old, respectively. In contrast, less than 10% mortality was observed in plots 1982B, 1985B, 1986A, 1986C, 1987Aand 1988A, while no mortality at all was observed in plot 1985C. It was clear that the occurrence of root disease was not uniform and that mortality rates differed from plot to plot. Similar variation in mortality rates had also been observed in the 1995 survey of root rot in A. mangium provenance trials in various parts of Peninsular Malaysia (Lee, 1997).

3 Current Status of Root Diseases of Acacia mangium 73 The rate of spread of the disease in the different plots was also variable. Mapping and regular monitoring of the trees showed that the disease most probably spread by root contact. In most cases, the initial disease foci enlarged Fig Mortality rates of Acacia mangium trees in Kemasul, Pahang, Peninsular Malaysia: (a) in the 1982, 1984 and 1985 plots; (b) in the 1986, 1987 and 1988 plots.

4 74 S.S. Lee Fig Distribution of dead and dying trees in plot 1988C: r, living trees; 1 6, dead and dying trees at the six sampling times; S, trees missing during plot establishment. with each passing year; this was clearly evident in all the 1984 plots and in plots 1987B and 1988C (Fig. 5.2). The absence of tree mortality in plot 1985C, even 13 years after planting, was not unexpected, as no root disease symptoms were observed on any of the trees in the plot during the duration of the study. While no symptoms of root disease were evident on the trees in plots 1985A, 1985B, 1986A, 1987A and 1988Aat the time of plot establishment, they started to appear 2 3 years after the study commenced. This suggests that the trees only became infected when their expanding root systems encountered some buried source of root disease inocula. As in the other plots mentioned earlier, the rate of disease spread was variable, with moderate increases in mortality in plots 1985A, 1986B, 1987C and 1988B, and very little increase in plots 1985B, 1986A, 1986C, 1987A and 1988A. The mortality of trees generally increased with time in plots where root disease was already present at plot establishment. The rate of disease spread was probably dependent on the presence, abundance and distribution of root disease inocula at the site, rate of root growth, extent of the root system of each tree, and extent of root contact between healthy and infected trees. These plantations had been established on logged-over lowland rainforest areas, which had been mechanically cleared and burned before planting. However, old tree stumps were still evident in the plots and it is highly likely that roots and other woody debris that harbour the facultative parasitic root-rot fungi remain buried in the soil, acting as sources of infection.

5 Current Status of Root Diseases of Acacia mangium 75 Fungi Associated with Root Diseases of A. mangium Based on the appearance of the infected roots, two main types of root diseases could be distinguished even though the visible disease symptoms on the tree crowns were similar. These were red-root disease and brown-root disease. Roots of trees infected by red-root disease are characteristically covered by a wrinkled, reddish-brown mycelial mat. The red colour of the mycelial mat becomes very evident when the root is washed clean of soil. Awhite mottling pattern is evident on the underside of the infected root and there is a very characteristic odour. In the early stages of infection, the wood remains hard and no colour change is discernible, but in advanced stages the wood becomes pale buff and spongy or dry, depending on the soil conditions. Red-root disease was the most frequently observed type of disease when roots were sampled. The characteristics of the disease are very similar to that of red-root disease caused by Ganoderma philippii (= G. pseudoferreum) on rubber (Anonymous, 1974). In brown-root disease, the roots are encrusted in a mass of earth and sand, intermingled with rusty brown patches. Advanced stages of the disease are easily recognized by the production of brown zigzag lines in the wood, forming a honeycomb-like pattern, and the wood becoming friable, light and dry. The brown lines are ridges of golden-brown fungal mycelium and the type of rot produced is known as pocket rot. These characteristic features indicate that the fungus associated with the disease is Phellinus noxius (Anonymous, 1974). The identity of the associated fungi could not be confirmed initially because of the absence of sporocarps on diseased or dead trees. Samples of diseased roots were thus collected for isolation of the associated fungi. Attempts were made to identify the pure-culture mycelial isolates by comparison with the species codes developed by Nobles (1965) and Stalpers (1978) and by inoculation onto wood blocks for the production of sporocarps (Lee and Noraini Sikin, 1999). For production of sporocarps on wood blocks, pure-culture isolates of the test fungi were first grown on malt agar (DIFCO Laboratories, USA) in the dark at ambient room temperature for about 1 week. In the meantime, blocks of debarked rubber wood, measuring 10 cm by 5 6 cm diameter, were placed individually into autoclavable plastic bags, wetted with approximately 50 ml of 2% malt extract and sterilized. Three 1 cm diameter plugs, taken from the edge of 1-week-old actively growing cultures, were then used to inoculate each rubber-wood block. Five replicate blocks were inoculated with each fungus and the inoculated blocks incubated in the dark at ambient room temperature (28 ± 2 C). At the end of 2 months the well-colonized blocks were removed from their plastic bags and planted into polybags containing unsterilized garden soil, one block per bag. These were then transferred to a shade house and lightly sprayed with tap water daily to keep the soil and the wood blocks moist. When sporocarps were produced, between 2 and 3 weeks later, they were collected for identification in the laboratory.

6 76 S.S. Lee The identity of the fungus associated with red-root disease could not be confirmed from the wood-block technique as no sporocarps were produced. However, the characteristic red skin of mycelium on the root is similar to that reported for G. philippii (= G. pseudoferreum) on rubber (Anonymous, 1974). From isozyme analysis, four isolates of Ganoderma obtained from A. mangium in West Malaysia were determined to be different from those isolated from palm hosts (Miller et al., 1995). Recently many sporocarps of G. philippii (Corner, 1983) were found growing on dead 10-year-old A. mangium trees in a plantation at Bidor, Perak. Inspection of trees with symptoms of root disease located close to the clumps of dead trees revealed that the roots were covered by a red mycelial mat (S. Ito, Bidor, 1999, personal communication), characteristic of red-root disease observed on A. mangium trees in Kemasul, Pahang and elsewhere. However, attempts to isolate the fungus, from both sporocarps and infected roots, were unsuccessful. Corner (1983) noted that G. philippii is rather common and distributed from Burma (Myanmar) to the Solomon Islands, being found on dead stumps in the forest and in the open, and parasitic on roots of trees, especially Hevea. Using the wood-block technique, sporocarps produced from mycelial isolates obtained from samples with brown-root disease were confirmed as those of P. noxius (Pegler and Waterston, 1968). Inoculated wood blocks also had the characteristic pocket rot similar to that observed on the diseased roots, indicative of rot caused by P. noxius. Some roots were covered by a thin, black crust, which was easily mistaken for necrotic tissue. The black crust was usually found on the roots of dead trees where the wood had become yellowish-cream in colour, spongy and light. Using the wood-block technique, hyphal isolates obtained from the black crust yielded sporocarps, identified as Amauroderma parasiticum (Corner, 1983). In addition to the root diseases reported here, a root disease associated with the presence of white rhizomorphs of an unidentified fungus has also been reported from A. mangium in Peninsular Malaysia (Lee, 1997). However, this disease was not observed during the present study. Pathogenicity Tests Pathogenicity tests are presently being conducted on A. mangium saplings in the FRIM nursery, and only preliminary results are reported here. Six-monthold A. mangium plants were transplanted into large polybags (33 cm depth by 35.5 cm diameter) containing a 1 : 1 mixture of forest soil and padi husk (this is the potting mixture normally used in the FRIM nursery). After the plants had become well established, about 3 months later, they were inoculated using branches (8 cm long by 1.5 cm diameter) of a rubber tree which had been well colonized by the test fungi (the rubber-tree branches, with intact bark, were inoculated using the same technique as described above for the inoculation of the rubber-wood blocks). Three well-colonized branches were used to

7 Current Status of Root Diseases of Acacia mangium 77 inoculate each test plant, with the branches buried in close proximity to the roots of the plant in the polybag. There were three replicates for each fungus and the fungal isolates tested were P. noxius, the suspected Ganoderma and A. cf. parasiticum. About 2 months after inoculation, symptoms of root disease were obvious on the plants inoculated with P. noxius and the suspected Ganoderma, while those inoculated with A. cf. parasiticum remained symptomless. However, different symptoms of root disease were observed on the plants inoculated with P. noxius and the suspected Ganoderma. Those inoculated with P. noxius exhibited progressive yellowing of the phyllodes, beginning with the tips of the younger phyllodes, resulting ultimately in defoliation and death of the infected plant. On the other hand, plants inoculated with the suspected Ganoderma suddenly wilted without any yellowing symptoms, and died within 5 days after the first symptoms were noticed. Roots of plants inoculated with the suspected Ganoderma were covered by a red mycelial mat but the fungus could not be successfully re-isolated from the affected plants. This experiment is being repeated to confirm the results presented here. Pathogenicity of P. noxius was proven as the fungus was successfully re-isolated from roots of the inoculated plants, which had rusty brown patches under a crust of soil. Plants inoculated with A. cf. parasiticum remained healthy even 6 months after inoculation. It would appear that this fungus is not a primary pathogen of A. mangium, but probably a secondary pathogen or weak parasite infecting stressed trees or trees which have been weakened or killed by some other agents. Corner (1983) recorded A. parasiticum as a parasite on the trunk of a living tree of Knema (Myristicaceae) in a swamp forest in Singapore. Conclusion Large-scale burning has been a common feature of land clearing in South-East Asia for conversion of forest or old tree stands into agricultural and industrial plantations, or for replanting. In 1997 large-scale burning for land clearing, and uncontrolled bush fires on the islands of Sumatra and Kalimantan in Indonesia, resulted in severe atmospheric pollution which lasted for several months over Singapore, Brunei, southern Thailand and large parts of Indonesia and Malaysia. Widespread public outcry and political pressure from regional governments resulted in the government of Indonesia declaring a no burn policy for land clearing, with the imposition of hefty fines for those found guilty of the offence. However, enforcement remains problematic. In Malaysia, the Environmental Quality (Clean Air) Regulations 1978 prohibit open burning, but in the past open burning for land conversion and replanting could be carried out under special contravention licences issued by the Department of Environment. The large-scale adoption of the zero burning

8 78 S.S. Lee technique by oil-palm plantation companies in Malaysia in 1989 has allowed oil-palm replanting to be done without violating the Environmental Quality (Clean Air) Regulations 1978, and the technique has also been developed for the replanting of oil palm and other plantation crops from logged-over forests (Golden Hope Plantations Berhad, 1997). In the aftermath of the 1997 haze, the Malaysian government issued a directive prohibiting almost all forms of open burning, and a law pertaining to this issue is presently under consideration by the Attorney-General s chambers. While zero burning is environmentally friendly and results in total recycling of plant tissues (the existing trees are felled, shredded and left to decompose in situ), it also gives rise to several problems, such as increased insect infestation and increased sources of root disease inocula. From the disease point of view, the woody residues act as potential reservoirs and food resources for the facultative parasitic root-disease fungi which live in the soil. In second-rotation A. mangium plantations in Sumatra, where no burning was carried out before replanting, there are already indications that losses due to root diseases will be much more serious, with a higher incidence of the disease in the young plantations and mortality occurring in younger plants. A. mangium trees as young as 6 months old have been observed to be killed by red-root disease (unpublished data) in such areas. In view of the potential damage and losses that can be caused by root diseases in A. mangium plantations, especially with the implementation of the zero burning / no burn policy by several South-East Asian governments, it is important that further research be conducted to determine the sources of inoculum, factors promoting the occurrence and spread of the disease, and methods for prevention, management and control of the disease. References Almonicar, R.S. (1992) Two types of root rot diseases affecting Acacia mangium. Nitrogen Fixing Tree Research Reports 10, Anonymous (1974) Root diseases Part 1: Detection and recognition. Planters Bulletin 133, Arentz, F. (1986) Forest Pathology Lecture Notes. Papua New Guinea Forestry College, Bulolo. Arentz, F. and Simpson, J.A. (1988) Root and butt rot diseases of native plantation species in Papua New Guinea. Paper presented at the Fifth International Congress of Plant Pathology. Kyoto, Japan. Corner, E.J.H. (1983) Ad Polyporaceas I. Amauroderma and Ganoderma. Nova Hedwigia 75, Golden Hope Plantations Berhad (1997) The zero burning technique for oil palm cultivation. Golden Hope Plantations Berhad, Kuala Lumpur. Khamis, S. (1982) Pests and diseases of forest plantation trees with special reference to SAFODA. In: Proceedings of the Eighth Malaysian Forestry Conference, Kota Kinabalu, pp

9 Current Status of Root Diseases of Acacia mangium 79 Lee, S.S. (1985) Tree Diseases and Wood Deterioration Problems in Peninsular Malaysia. Occasional Paper No. 5, Serdang: Faculty of Forestry, Universiti Pertanian Malaysia. Lee, S.S. (1993) Diseases. In: Kamis Awang and Taylor, D. (eds) Acacia mangium Growing and Utilization. MPTS Monograph Series No. 3. Winrock International and FAO, Bangkok, Thailand, pp Lee, S.S. (1997) Diseases of some tropical plantation acacias in Peninsular Malaysia. In: Old, K.M., Lee, S.S. and Sharma, J.K. (eds) Diseases of Tropical Acacias. Proceedings of an International Workshop, Subanjeriji, South Sumatra, 28 April 3 May CIFOR Special Publication, Bogor, pp Lee, S.S. and Noraini Sikin Yahya (1999) Fungi associated with heart rot of Acacia mangium trees in Peninsular Malaysia and Kalimantan. Journal of Tropical Forest Science 11(1), Miller, R.N.G., Holderness, M., Bridge, P.D., Paterson, R.R.M., Hussin, M.Z. and Sariah Meon (1995) Isozyme analysis for characterization of Ganoderma strains from south-east Asia. Bulletin OEPP/EPPO Bulletin 25, Millitante, E.P. and Manalo, M.Q. (1999) Root rot disease of mangium (Acacia mangium Willd.) in the Philippines. Poster. Fifth International Conference on Plant Protection in the Tropics, Kuala Lumpur, Malaysia, March 1999, pp Nobles, M.K. (1965) Identification of cultures of wood-inhabiting Hymenomycetes. Canadian Journal of Botany 43, Old, K.M., Lee, S.S. and Sharma, J.K. (eds) (1997) Diseases of Tropical Acacias. Proceedings of an International Workshop, Subanjeriji, South Sumatra, 28 April 3 May CIFOR Special Publication. Pegler, D.N. and Waterston, J.M. (1968) Phellinus noxius. Commonwealth Mycological Institute Descriptions of Pathogenic Fungi and Bacteria No Stalpers, J.A. (1978) Identification of Wood-inhabiting Aphyllophorales in Pure Culture. Studies in Mycology No. 16. Centraalbureau voor Schimmelcultures, Baarn. Turnbull, J. (ed.) (1986) Australian Acacias in Developing Countries. Proceedings of an International Workshop held at the Forestry Training Centre, Gympie, Queensland, Australia, 4 7 August ACIAR Proceedings No. 16. Yap, S.K. (1986) Introduction of Acacia species to Peninsular Malaysia. In: Turnbull, J. (ed.) Australian Acacias in Developing Countries. Proceedings of an International Workshop held at the Forestry Training Centre, Gympie, Queensland, Australia, 4 7 August ACIAR Proceedings No. 16, pp