Pathogen & Distribution
Armillaria is a globally distributed fungus that is abundant across natural forests and managed landscapes (Sinclair and Lyon 2005; Kim et al. 2022). It is one of the most important decay pathogens of trees and shrubs and has played a role in the death of an untold number of trees (Wargo and Shaw 1985). Of the approximately 40 recognized species of Armillaria (Kim et al. 2022), six occur in New England: A. calvescens, A. gallica, A. gemina, A. mellea, A. sinapina, and A. solidipes (Brazee and Wick 2009, 2011). Armillaria preferentially attacks weakened and stressed trees, with drought and insect defoliation the most common predisposing stresses (Wargo 1996; Sinclair and Lyon 2005). While its role as a pathogen of forest trees is well documented, Armillaria can also be particularly abundant in parks and botanical gardens (Drakulic et al. 2017; Cromey et al. 2020). In urban centers, the pathogen is less common but still occurs (Luley 2022). In addition to being a major forest pathogen, Armillaria also has an important ecological role by recycling nutrients as a decomposer and removing weak and suppressed trees (Kim et al. 2022).
Host Range
Nearly all woody plants and even some non-woody plants are susceptible to infection from Armillaria (Sinclair and Lyon 2005; Cromey et al. 2020). In the northeast, certain Armillaria species more frequently attack conifers (e.g. A. solidipes) while others prefer hardwoods (e.g. A. gallica), but most can be found attacking both conifers and hardwoods (Brazee and Wick 2009, 2011). The age and health of the host tree or shrub can significantly influence their ability to resist infection. Common hosts in managed landscapes across southern New England include maple (Acer) and oak (Quercus). The disease is also common at Christmas tree farms on true fir (Abies).
Symptoms & Signs
Aboveground symptoms of Armillaria root and butt rot are often very general and may include upper canopy dieback, stunted shoots and undersized foliage, excessive seed or cone production, browning leaves or needles especially after periods of drought, excessive tapering of the lower trunk (basal flaring), sap/resin flow and cracks on the lower trunk, and basal cavities (Sinclair and Lyon 2005). Young trees can be killed relatively quickly after infection due to a lack of natural defenses. Well-established, mature trees may be infected by Armillaria for decades without showing major symptoms until they are weakened by drought or defoliation. In other cases, trees may never show symptoms but suffer from stem failure or uprooting under loading from strong winds due to the structural instability caused by decay (Schwarze et al. 2000). Once the tree dies, Armillaria lives as a saprophyte, decomposing the infected wood tissue and producing large masses of rhizomorphs. The primary modes of dispersal are through rhizomorphs and root grafts (root to root contacts) between diseased and healthy trees.
Rhizomorphs are complex, root-like filaments of fungal tissue (mycelia) that are encased in a black, melanized rind (Fox 2000). Rhizomorphs can grow through the soil until they encounter nearby roots or the lower trunk of a susceptible tree. The rhizomorphs then attach to the bark where they can either remain somewhat dormant or invade through chemical and physical means to attack cambial tissues that are rich in sugars (Devkota and Hammerschmidt 2020). A large mass of rhizomorphs may develop on the root bark before the fungus invades the host tree, therefore their presence alone does not indicate an active infection (Devkota and Hammerschmidt 2020; Luley 2022). A buildup of rhizomorphs on the roots allows the fungus to readily cause disease once trees are stressed by drought and defoliation (Marçais and Bréda 2006).
Mycelial fans are white-colored sheets of fungal mycelia (the body or thallus of the fungus). They develop under the bark and when advanced infections are present, they can be revealed through careful removal of the bark from the underlying sapwood (Sinclair and Lyon 2005; Luley 2022). On living trees suspected of being infected by Armillaria, excavation of the root flare and examination of large, lateral roots under the soil surface may reveal decaying wood with embedded mycelial fans. A knife or small hand tool can be used to look for decaying sections of lateral roots before removing bark to determine if mycelial fans are present.
Armillaria produces annual mushrooms from late summer to fall at the base of stumps or recently killed trees (Luley 2022). They may appear from late August through October, but in southern New England they are most abundant during a relatively short period in late September and early October. These gilled mushrooms typically grow in dense clusters, have caps that are golden tan to brown in color, and often have a conspicuous ring on the white stem (Fox 2000). When young, there may be scales on the surface of the cap that disappear with age. Spores are locally wind-dispersed and can initiate new infections. This is a concern across managed landscapes such as parks and botanical gardens where basal wounds are common (Travadon et al. 2012). Mushroom production can be sporadic, often occurs long after the infected tree is dead, and is therefore not a reliable indicator of pathogen presence (Luley 2022).
Damage & Pattern of Decay
Armillaria is a white rot pathogen, meaning it can decay lignin, cellulose and hemicellulose in the cell walls of woody tissues (Blanchette 1991; Luley 2022). But it does not decay each type at the same time. Microscopic examination has shown that A. mellea preferentially decays cell walls that are relatively low in lignin content, instead targeting cellulose and hemicellulose (Schwarze et al. 2000a, 2000b; Schwarze 2007). When additional species (A. borealis, A. cepistipes, A. gallica, and A. ostoyae) were examined, most also preferentially targeted cellulose and hemicellulose first, avoiding heavily lignified cell walls (Schwarze 2007). The exception was A. gallica, which was capable of a simultaneous decay of lignin, cellulose and hemicellulose. This latter point about A. gallica is particularly relevant as itis the most common species in southern New England and abundant as a butt rot pathogen of oaks (Brazee and Wick 2009, 2011). When cellulose and hemicellulose are targeted first, the decaying wood may have a light brown discoloration (Sinclair and Lyon 2005).
When the decay becomes advanced, Armillaria can break down more heavily lignified cell wells, and the wood tissue becomes bleached, fibrous to spongy, often separating longitudinally (Schwarze et al. 2000b). This pattern of decay, where lignin degradation takes place after cellulose and hemicellulose are targeted, means that during the early stages of decay Armillaria may better resemble some soft rot pathogens (e.g. Kretzschmaria) and even brown rot pathogens (e.g. Laetiporus). Ultimately, soft rot and brown rot pathogens cause only minor lignin degradation or modification, while rot fungi like Armillaria are capable of significant lignin breakdown (Schwarze et al. 2000b).
Wood colonized by Armillaria may have numerous black zone lines (pseudosclerotial plates) interspersed throughout. These zone lines often demarcate healthy and decaying wood and are somewhat diagnostic, but also regularly produced by Kretzschmaria (Schwarze et al. 2000) and Phellinus (Sinclair and Lyon 2005). Wood in an advanced state of decay is often water soaked and studies have shown Armillaria can decay wood under very low oxygen levels (Schwarze et al. 2000b).
Armillaria exhibits two patterns of host colonization and decay, and they may happen at the same time. The first is when the phloem, cambium and outer sapwood are attacked, creating lesions that may result in a gradual canopy dieback with no extensive decay developing in the heartwood (Sinclair and Lyon 2005). The second is when the decay occurs entirely within the heartwood and there are no or few visible symptoms of the damage (Kile et al. 1991). The decay can slowly expand outward into live sapwood over time, resulting in a general dieback or trees may suffer root or stem failure under loading from strong winds. Determining which pattern of decay is present can be an important factor for management.
Detection & Management
Confirm the presence of Armillaria through symptoms, signs, and the pattern of wood decay, if possible. Keep in mind that rhizomorphs attached to the outer root bark do not always indicate active infections. Minimally invasive detection techniques, such as resistance drilling or sonic tomography, are often required to understand the extent of the damage. Yet, even with advanced detection methods, determining the extent of root damage is often impossible. Infected trees should receive a thorough risk assessment before any considerations on removal are made. Additionally, keep in mind that co-occurring infections with other decay fungi (e.g. Grifola frondosa and Laetiporus sulphureus) are possible, sometimes confounding the identification process.
Root flare excavation and careful examination of primary lateral roots for decay can be helpful in detecting the pathogen and corroborating aboveground symptoms. Root collar excavation has also been shown to reduce disease incidence and mortality in orchard settings (Schnabel et al. 2012; Miller et al. 2020). By exposing the flare and lateral roots, rhizomorphs and mycelial fans that would be protected under the soil are exposed to natural elements and desiccation. A reduced number of rhizomorphs on the flare would make natural defense by the host more likely.
Armillaria grows very slowly, and infected trees may persist and remain structurally stable for many years to decades. Maintaining high tree vigor is the best course of action when the fungus is known to be present. Healthy trees frequently resist attack and compartmentalize infections by Armillaria and only succumb to advanced decay and death when they are weakened by other stresses (Sinclair and Lyon 2005). When decay in the heartwood is present, trees may endure if their annual increment growth can keep pace with the rate of internal decay. Avoid drought stress by providing supplemental water during extended dry periods. Fertilization, maintaining optimal soil pH, and avoiding needless physical wounding from mowers and string trimmers will also promote vigor and aid natural defenses against Armillaria. Maintaining a large, mulched area around the tree will limit wounding to lateral roots, moderate soil temperatures, and reduce competition for moisture with turfgrasses. Protect infected trees from defoliating insect outbreaks as this is one of the primary stresses that facilitates disease development.
Chemical control of Armillaria is generally not recommended. Because the pathogen lives within woody tissues or in the soil, applied chemicals often become bound to soil colloids or are leached away without ever reaching the fungus. That said, phosphites are one chemical that may provide some utility, although its efficacy will be very difficult to quantify. A lower trunk spray or soil drench in the immediate root zone can be performed to help slow disease development for trees experiencing a general decline. Phosphites are highly mobile in the vascular system, moving bidirectionally within the treated plant (Thao and Yamakawa 2009). While only weakly fungicidal, phosphites can stimulate the tree’s natural defense response, which can be valuable against a slow-growing, native pathogen like Armillaria.
Because Armillaria can persist for many years as a saprophyte on stumps and large lateral roots, stump grinding and removal of wood chips is recommended in some cases. Avoidance of Armillaria is difficult, due in part to the widespread distribution of the pathogen. Its ability to produce a vast melanized rhizomorph network that grows undetected through the soil in search of a new host is a major advantage over other wood-rotting fungi. Even with good care, Armillaria can play an important role in the decline and death of trees in managed landscapes.
Citations
Blanchette RA. 1991. Delignification by wood-decay fungi. Annual Review of Phytopathology 29(1) 381–403. https://doi.org/10.1146/annurev.py.29.090191.002121
Brazee NJ and Wick RL. 2009. Armillaria species distribution on symptomatic hosts in northern hardwood and mixed oak forests in western Massachusetts. Forest Ecology and Management 258(7): 1605–1612. https://doi.org/10.1016/j.foreco.2009.07.016
Brazee NJ and Wick RL. 2011. Armillaria species distribution and site relationships in Pinus- and Tsuga-dominated forests in Massachusetts. Canadian Journal of Forest Research 41(7): 1477–1490. https://doi.org/10.1139/x11-076
Cromey MG, Drakulic J, Beal EJ, Waghorn IAG, Perry JN, and Clover GRG. 2020. Susceptibility of garden trees and shrubs to Armillaria root rot. Plant Disease 104(2): 483–492. https://doi.org/10.1094/PDIS-06-19-1147-RE
Devkota P and Hammerschmidt R. 2020. The infection process of Armillaria mellea and Armillaria solidipes. Physiological and Molecular Plant Pathology 112: 101543. https://doi.org/10.1016/j.pmpp.2020.101543
Drakulic J, Gorton C, Perez-Sierra A, Clover G, and Beal L. 2017. Associations between Armillaria species and host plants in U.K. Gardens. Plant Disease 101(11): 1903–1909. https://doi.org/10.1094/PDIS-04-17-0472-RE
Fox RTV. 2000. Biology and life cycle. Pp. 3–44 In: Armillaria Root Rot: Biology and Control of Honey Fungus. Intercept Ltd, Andover, United Kingdom.
Kile GA, McDonald GI, and Byler JW. 1991. Ecology and Disease in Natural Forests. Pp. 102–121 In: Shaw CG and Kile GA (eds). Armillaria Root Disease. USDA Forest Service Agricultural Handbook No. 691.
Kim MS, Heinzelmann R, Labbé F, Ota Y, Elías-Román RD, Pildain MB, Stewart JE, Woodward S, and Klopfenstein NB. 2022. Armillaria root diseases of diverse trees in wide-spread global regions. Pp. 361–378 In: Asiegbu FO and Kovalchuk A (eds). Forest Microbiology, Vol. 2: Forest Tree Health. Academic Press, London, UK. https://doi.org/10.1016/B978-0-323-85042-1.00004-5
Luley CJ. 2022. Armillaria mellea. Pp. 34–37 In: Wood Decay Fungi Common to the Northeast & Central United States, 2nd edn. Urban Forest Diagnostics LLC, Naples, NY.
Marçais B and Bréda N. 2006. Role of an opportunistic pathogen in the decline of stressed oak trees. Journal of Ecology, 94: 1214–1223. https://doi.org/10.1111/j.1365-2745.2006.01173.x
Miller SB, Gasic K, Reighard GL, Henderson WG, Rollins PA, Vassalos M, and Schnabel G. 2020. Preventative root-collar excavation reduces peach tree mortality caused by Armillaria root rot on replant sites. Plant Disease 104(5): 1274–1279. https://doi.org/10.1094/PDIS-09-19-1831-RE
Schnabel G, Agudelo P, Henderson GW, and Rollins PA. 2012. Above-ground root collar excavation of peach trees for Armillaria root rot management. Plant Disease 96(5): 681–686. https://doi.org/10.1094/PDIS-06-11-0493
Schwarze FWMR, Baum S, and Fink S. 2000a. Resistance of fibre regions in wood of Acer pseudoplatanus degraded by Armillaria mellea. Mycological Research 104(9) 1126–1132. https://doi.org/10.1017/S0953756200002525
Schwarze FWMR, Engels J, and Mattheck C. 2000b. Fungal Strategies of Wood Decay in Trees. Springer, Berlin, Germany. https://doi.org/10.1007/978-3-642-57302-6
Schwarze FWMR. 2007. Wood decay under the microscope. Fungal Biology Reviews 21: 133–170. https://doi.org/10.1016/j.fbr.2007.09.001
Sinclair WA and Lyon HH. 2005. Armillaria Root Rots. Pp. 326–331 In: Diseases of Trees and Shrubs, 2nd edn. Cornell University Press, Ithaca, NY.
Thao HTB and Yamakawa T. 2009. Phosphite (phosphorous acid): Fungicide, fertilizer or bio-stimulator? Soil Science and Plant Nutrition 55(2): 228–234. https://doi.org/10.1111/j.1747-0765.2009.00365.x
Travadon R, Smith ME, Fujiyoshi P, Douhan GW, Rizzo DM, and Baumgartner K. 2012. Inferring dispersal patterns of the generalist root fungus Armillaria mellea. New Phytologist 193(4): 959–969. https://doi.org/10.1111/j.1469-8137.2011.04015.x
Wargo PM. 1996. Consequences of environmental stress on oak: predisposition to pathogens. Annals of Forest Science 53(2–3): 359–368. https://doi.org/10.1051/forest:19960218
Wargo PM and Shaw CI. 1985. Armillaria root rot: the puzzle is being solved. Plant Disease 69(10): 826–832. https://doi.org/10.1094/PD-69-826