Biology, Ecology, and Epidemiology of Heterobasidion annosum

Pertinent literature on the biological aspects of annosus root disease is reviewed. Key features of the life cycle of Heterobasidion annosum such as stump infection, stump colonization, host-parasite relations, and interactions of various physical and biological factors are discussed in relation to forest stands in the western United States. This review suggests our knowledge of the pathology of this disease is limited on most affected tree species. Further research on various aspects of the life cycle of this fungus is essential to minimizing losses to this disease. The literature on Heterobasidion annosum (Fr.) Bref. before 1970 contains over 1,000 titles dealing with various aspects of the fungus and the disease it causes (Hodges and others 1971; Koenigs 1960). A preliminary literature review conducted by Otrosina estimates at least 850 titles dealing with H. annosum have been published during the period 1970 to 1988. This paper is not intended to be a review and will not attempt to address all aspects of the biology of H. annosum; it will highlight pertinent research on the biological and ecological relationships as they pertain to the pathology of pine and true fir in the western coastal states of the United States. The disease as it relates to other hosts in other geographic areas is discussed elsewhere in these proceedings. STUMP SUSCEPTIBILITY AND INFECTION The most crucial stage in the disease cycle of H. annosum is the entry or invasion of the fungus into the stand where it can then move from tree to tree through roots. The primary mode of stand entry in pines is through freshly cut stump surfaces (Begs 1963) (fig. 1). We believe that stump infection is important in fir as well, 1 Presented at the Symposium on Research and Management of Annosus Root Disease in Western North America, April 18-21, 1989, at Monterey, California. 2 Research Plant Pathologist, Pacific Southwest Forest and Range Experiment Station, Berkeley, California; and Professor, Department of Plant Pathology, University of California, Berkeley. though there are other modes of entry in Abies (fig. 2). Stump surfaces act as ideal semiselective media for germination of deposited basidiospores of the fungus. Susceptibility of stump surfaces of various hosts has been studied by a number of investigators (Rishbeth 1951; Yde-Andersen 1962; Cobb and Barber 1968). The general consensus of these studies is that stumps of most susceptible species can remain receptive to invasion by the fungus for up to 45 days, depending upon season and host species. On the other hand, Cobb and Schmidt (1964) found eastern white pine (Pinus strobus L.) stumps to be highly susceptible for only a few days after felling. In the western United States, ponderosa pine (Pinus ponderosa Laws.) stumps may remain susceptible for at least 4 weeks, although susceptibility drops markedly after 1 to 2 weeks (Cobb and Barber 1968). Susceptibility of stumps also was greater in the autumn than in the spring. This was attributed to higher resin content of cut stump surfaces in the spring-felled trees than in those felled in the fall. Not all susceptible tree species are colonized through stump surfaces at the same rates or conditions as ponderosa pine. For example, spore inoculation studies of incense cedar (Calocedrus decurrens (Torr.) Florin) suggest substantially more resistance to colonization under the same conditions that allow ponderosa pine stumps to be colonized (Hunt and others 1974). Temperature is an important factor in determining successful infection of stump surfaces by H. annosum. The optimal temperature for growth of the fungus in pure culture is 23-26 C for a wide variety of host and geographic origins of isolates (Cowling and Kelman 1964). The fungus is also capable of considerable growth at lower temperatures, averaging 21 percent of optimum at 8 C. In general, the fungus does not grow at temperatures above 32 C. The upper temperature limit has important implications regarding stump infection in certain climates. Ross (1969) found basidiospores and conidia of the fungus to be inactivated after 60 minutes at temperatures above 45 C. There is an apparent difference in temperature effects between mycelia and spores. Actively growing mycelia can become inactive or killed at temperatures above 35 C (Gooding 1964). In California, stumps in ponderosa pine stands may be exposed to temperatures greater than 35 C during the summer months. For example, Cobb and Barber (1968) noted ambient temperatures greater than 33 C during a study involving artificial inoculation of stumps, but they detected stump 26 USDA Forest Service Gen. Tech. Rep. PSW-116 infection by H. annosum during this period of high temperature. They so found that sumps exposed to direct solar radiation in stand openings were infected at the same level as stumps under more closed canopies. In the southeastern United States, recommendations for controlling annosus root disease in southern pine stands revolve around thinning stands in the warm summer months, during which ambient temperatures are above the 35 C inactivation point for the fungus (Ross 1973). Studies conducted by Cobb and Barber (1968), Gooding (1964), and Rose and others (1980) suggest high stump temperatures may not be the sole factor responsible for lowering rates of stump infection. Gooding (1964) studied survival of H. annosum in inoculated bolts of loblolly pine (Pinus taeda L.) incubated at various temperatures. He was unable to recover the fungus from bolts incubated at 35 C and above that were not surface sterilized before inoculation. On surface sterilized bolts, however, the fungus was reisolated at temperatures up to 40 C. These results suggest microbial activity at the stump surface plays some synergistic or interactive role in stump infection at higher temperatures. Rapid replacement of H. annosum by Trichoderma viride Pers. ex Fr. in a greenhouse inoculation study was attributed to high soil temperatures (Towers and Stambaugh 1968). Also, T. viride may act together with other fungi such as the saprotrophic colonizer Phlebia (Peniophora) gigantea (Fr.) Masses to inhibit H. annosum (Curl and Arnold 1964). The stump infections observed in California during the hot, dry summer months may indicate differences in kinds and quantity of microorganisms present on stump surfaces between climatic and geographic regions. The warm, humid climate of the southeastern United States tends to favor fungi such as Trichoderma and Phlebia, where they can often be observed fruiting on stump surfaces. However, these fungi are rarely observed in this manner in California. The inoculum potential of the fungus in the form of airborne spores (largely basidiospores) is another important determinant of stump infection. Spore deposition rates have been measured almost everywhere annosus root disease is a problem. Edmonds and others (1984) found deposition rates in precommercially thinned stands of western hemlock (Tsuga heterophylla (Raf.) Sarg.) to be up to 8 times greater (up to 19,577/m/hr) in Figure 1--Infection cycle of Heterobasidion annosum in Pinus. USDA Forest Service Gen. Tech. Rep. PSW-116 27 Figure 2--Infection cycle of Heterobasidion annosum in Abies. precommercially thinned than in commercially thinned stands. In California, spore deposition rates in mixed conifer forests ranged from 3 to 796 spores/m/hr, depending on geographic location and season (James and Cobb 1984). Generally, the highest rates occurred in the autumn in these forests whereas in the southeastern United States, greatest spore deposition rates are observed during the winter months (Drummond and Bretz 1967; Ross 1969). Because H. annosum has an asexual spore state, Oedocephalum lineatum Bakshi (=Spiniger meineckellus (Olson) Stalpers), the question has arisen as to its function in nature, is., whether the asexual conidiospores are an important etiological agent. Kuhlman and Hendrix (1964) found conidial inoculum inferior to basidiospore inoculum as measured by stump colonization 9 months after inoculation with spore suspensions. They did not indicate the relative spore concentrations in their inoculum solutions, but check inoculations on pine disks indicated comparable initial viability of inocula. Conidial inoculum has been used successfully numerous times by others in the study of stump infection and colonization (James and others 1980b). Conidia have been shown to survive in field soils having extremely low water potentials for several months, although survival declines over time to a greater extent in sandy soils than in clay loans (Kuhlman 1969a). The potential for direct root infection by spores of H. annosum exists, and may be responsible for initiation of some root infections, particularly in injured stump roots created after felling (Kuhlman 1969b).