Root diseases in forest ecosystems^†

^†Contribution to the symposium “Root Diseases; Challenges and Perspectives” held during the Canadian Phytopathological Society Annual Meeting, 22–25 June 2009, Winnipeg, MB.

Abstract

The root system is an important part of a tree, but being inconspicuous it does not attract much attention. Therefore, root diseases are often invisible during much of the pathogens' life cycle. Nevertheless, they cause important losses due to mortality and reduced growth, but they are also components of forest ecosystems. For example, the complex of Armillaria root diseases, frequently associated with Armillaria ostoyae, attacks stressed trees and can kill seedlings or reduce the growth of trees during decades while hidden in roots. Inonotus tomentosus is common in spruce. From our observations, the pathogen usually infects trees older than 30 years; conifer seedlings planted on an infested site do not show any disease symptoms even after 10 years. Again, I. tomentosus needs stressed trees to develop in a stand. Heterobasidion annosum is an aggressive pathogen of pine. It colonizes fresh pine stumps after thinning in pine stands and can kill surrounding trees. Through lack of knowledge, foresters can create conditions conducive to the spread of root diseases: for example, precommercial thinning in the boreal forest has promoted Armillaria root diseases. Thinning in red pine plantations also creates an ecological niche favourable to H. annosum. Conversely, high-density spruce plantations will trigger Tomentosus root rot infestations. Proactive forest protection needs to integrate knowledge of silviculture, ecology, entomology and pathology. Understanding the ecology of these fungi is the first step.

Résumé: Le système racinaire est une partie importante mais peu visible de l'arbre; pour cette raison, on a tendance à l'oublier. Les maladies des racines sont aussi invisibles pendant une grande partie du cycle vital du champignon pathogène. Néanmoins, ces maladies sont responsables d'importantes pertes parce qu'elles causent de la mortalité et des réductions de croissance chez les arbres infectés. Toutefois, ces microorganismes constituent aussi une composante de l'écosystème forestier. Par exemple, le complexe des pourridiés-agarics, fréquemment associé à l'espèce Armillaria ostoyae, s'attaque aux arbres ayant subi un ou des stress; A. ostoyae peut tuer des semis en un an ou deux ou encore réduire la croissance des arbres pendant des décennies, tout en demeurant caché dans les racines. Inonotus tomentosus est pour sa part commun sur les épinettes. D'après nos observations, ce champignon pathogène infecte habituellement des arbres de plus de 30 ans; les semis de conifères plantés sur un site infesté par ce ravageur ne montraient pas encore de symptômes 10 ans après la plantation. Inonotus tomentosus a besoin d'hôtes stressés pour se développer dans un peuplement. Heterobasidion annosum est un champignon pathogène aggressif des pins. Il colonise les souches fraîchement coupées après les éclaircies dans les pinèdes et tue les arbres avoisinants. Sans le savoir, des forestiers peuvent créer des conditions propices aux maladies des racines : par exemple, des éclaircies précommerciales en forêt boréale ont favorisé le développement des pourridiés-agarics. L'éclaircie dans les plantations de pin rouge crée une niche écologique favorable à la colonisation par H. annosum. Au contraire, s'il n'y a pas d'éclaircie, un trop grand nombre de tiges à l'hectare peut provoquer une infestation de la carie rouge alvéolaire causée par I. tomentosus. La protection proactive des forêts doit intégrer les connaissances des spécialistes en sylviculture, en écologie forestière, en entomologie forestière et en pathologie forestière. Bien entendu, la compréhension de l'écologie des champignons pathogènes doit d'abord être bien comprise.

Keywords:

• Armillaria ostoyae
• Heterobasidion annosum
• Inonotus tomentosus
• root diseases

Mots clés:

• Armillaria ostoyae
• Heterobasidion annosum
• Inonotus tomentosus
• maladies des racines

Introduction

Over the years, my research has focussed on several forest pest problems such as stem decay, scleroderris canker (Gremmeniella abietina (Lagerberg) Morelet), and white pine blister rust (Cronartium ribicola J.C. Fish.), but also on root diseases such as Annosus root rot (Heterobasidion annosum (Fr.) Bref.) and Tomentosus root rot (Inonotus tomentosus (Fr.) Teng). While working with the Forest Insect and Disease Survey team at the Canadian Forest Service, I also had the opportunity to work on several other problems related to forest protection. For this reason, I am not strictly a specialist of root diseases. However, this broad experience in forest pathology gives me the opportunity, I believe, to have a better view of forest protection as part of the forest ecosystem.

The root system of a tree fixes and feeds the plant. As the crown of a tree is getting larger, foresters have a tendency to forget about the root system. Because of its location, the root system is inconspicuous. Nevertheless, it has to survive in its own environment surrounded by living organisms such as mycorrhizae, bacteria, insects and fungal pathogens. It must adapt itself to soil conditions, climatic changes and pollution (Manion, 1991).

If the root system does not draw much attention, neither do root diseases. Not only are root diseases often invisible during much of the pathogens' life cycle, but trees are also infected several years prior to showing any visible crown symptoms. By then it is too late for intervention; the growth of trees is too reduced and they will die.

Statistics in the annual report The State of Canada's Forests (Natural Resources Canada, 2008) provide information year after year on areas, in hectares, of forests defoliated by insects, and more recently on areas of beetle-killed trees and burned forest, both also in hectares. Unfortunately, based on this report, it seems that other problems related to forest protection that do not meet the criteria of surface affected on an annual basis are not included in the statistics and consequently they are not considered important by the readers. In spite of that, stem decay has been studied in eastern Canada and a compendium of research results has been published by Basham (1991). Several of these studies are also reporting losses caused by root diseases. Despite the fact that they are difficult to detect, losses due to mortality and reduced growth of trees caused by root diseases are some of the most important ones in our forests.

For example, in Ontario, where more data are available because research on root disease has been going on for several decades, the average annual volumes of losses due to mortality and growth reduction caused by root diseases alone are 8 020 432 m³ and 668 571 m³, respectively (Hall & Moody, 1994). These average out at 27% of the total loss caused by all pests (insects and diseases) in this province. This is just below the 31% loss caused by the spruce budworm for the 1982–1987 period which includes the peak of the spruce budworm epidemic in 1985. In the Pacific and Yukon region, the volume lost to root diseases is estimated at 5 477 780 m³. About three-quarters of this volume is attributable to tree mortality and most of it is caused by Armillaria root diseases (Hall & Moody, 1994).

These data show that root rots are a very important component of the ecosystem and that they are more harmful to our forests than other more conspicuous pests. Most of the time, as with other pests, it is possible to recognize a cascade of events leading to an epidemic. The last pest in this chain of events is not necessarily the most important one.

In the forest ecosystem, where lifespans are calculated in terms of decades instead of weeks for most crops, all pests and abiotic factors are important over the course of a tree's lifespan. With an ecosystemic approach in mind, I will briefly review three root diseases present in Canada. Then, I will look at these diseases as components of a forest and also as part of forest sciences. This vision should help everyone have a better understanding of the necessary collaboration between specialists in silviculture, forest ecology, forest entomology and forest pathology to improve the efficiency of forest protection.

Annosus root rot

Annosus root rot was first described in 1882 by the father of forest pathology, Robert Hartig, under the name Trametes radiciperda R. Hartig (Hartig, 1900). Since then hundreds of publications have been produced on the disease. The goal here is not to review the whole subject, but an update of our knowledge on H. annosum can be found in Woodward et al. (1998). Key information on the biology of the pathogen was published by Rishbeth (1951). We know from his observations that the disease invades a pine stand through fresh stump infection by H. annosum. Then the pathogen infiltrates the stumps and main roots, and finally spreads to the roots of surrounding living conifers and kills them, creating a circle of mortality. After thinning of a pine stand, the probability of having multiple centres of infection is very high as over 400 stems per hectare are removed and can potentially become many new centres of infection. Moreover, when the pathogen colonizes a site it can remain on that site for several years. For example, Greig & Pratt (1976) observed H. annosum living in stumps for periods of up to 62 years, and this is not the absolute maximum length of time. These infested sites cannot be reforested with any type of conifers without recording seedling mortality.

Heterobasidion annosum is an aggressive pathogen of pine. Findings by Rishbeth (1951) on the biology of the disease have made it possible to prevent infection through stump treatment. Different products have been tested to this effect and it was found that the biological agent Phlebiopsis gigantea (Fr.:Fr.) Jülich was and still is one of the best (Rishbeth, 1963). In eastern Canada, we have tested a few isolates of P. gigantea on red pine (Pinus resinosa Ait.) stumps under field conditions which led to an excellent control of the disease (Dumas & Laflamme, 2007; Laflamme & Dumas, 2007). Unfortunately, registration of such a product is very costly even if the quantity to be used is relatively small; nevertheless, tentative registration is underway.

Another possibility is to eradicate the disease by removing infected stumps. We have run one trial with some success, but infection centres must only cover a small area and the field work must be done under close supervision (Laflamme et al., 1998). Also, instead of one row, two rows of stumps from apparently healthy trees must be removed around the infection centre to increase the efficacy of the treatment.

In eastern Canada, Annosus root rot was first reported in the Niagara Peninsula in thinned red pine plantations (Hord & Quirke, 1955). Later, it was reported at Larose Forest near Ottawa (Sippell et al., 1968). In 1983, four thinned red pine plantations were selected on the Quebec side of the Ottawa River facing Larose Forest for yearly inspections that were done over a 10-year period. In 1989, the disease was found and the presence of H. annosum was confirmed in one of the plantations (Laflamme & Blais, 1995). The stump infections occurred in 1981 when thinning was carried out in the plantation, and mortality began seven to eight years later on trees surrounding the infected stumps. The disease is still spreading northward from there and is now reaching a region in Quebec where large natural stands of jack pine (Pinus banksiana Lamb.) are present. Obviously, these pines are an open target and could become infected too.

On the west coast of Canada, Annosus root rot is not present but it has been reported in the past. According to the new taxonomy, H. annosum is probably not present in British Columbia. The so-called S type for spruce has now been described as a new species named Heterobasidion parviporum Niemelä and Korhonen (Niemelä & Korhonen, 1998). In Europe, the new name for the F type for fir is now Heterobasidion abietinum Niemelä and Korhonen (Niemelä & Korhonen, 1998). Heterobasidion spp. are present in fir and spruce in the western USA, but as of yet we do not know for sure if they are the same species as those found in Europe (Korhonen et al., 2003).

In short, we know that it takes 8–10 years for H. annosum to kill trees near infected stumps. The disease is progressing right now in red pine plantations; it could soon be invading natural jack pine stands in the boreal forest. Annosus root disease is also progressing northward in western North America.

Tomentosus root rot

Inonotus tomentosus, also known under the name Onnia tomentosa (Fr.) P. Karst., is causing root diseases mainly in spruces across Canada, but it can also be found in other conifers.

One of the first studies on decay of black spruce was led by René Pomerleau in the province of Quebec, Canada, as early as 1939 (Lavallée, 1987). A total of 6000 black spruce were dissected between 1939–1944 and 1954–1957. Inonotus tomentosus was the most frequent root pathogen found with up to 33% and 31% of spruce affected in natural stands of the Charlevoix and Baie-Comeau regions, respectively. Later in his study on I. tomentosus, Whitney (1962) reported a stand-opening disease that was causing considerable losses in white spruce stands of Saskatchewan and Manitoba. Inonotus tomentosus was associated with 80% of the dead trees and 58% of the diseased trees in these stand openings. Reduction in growth beginning about 15 years prior to tree death was observed (Whitney, 1962).

We have noticed a similar pattern in a 50-year-old white spruce plantation in Harrington, Quebec where 85% of the trees were infected by I. tomentosus and mortality was detectable about 12–15 years after growth reduction had begun. However, when a sample of some living spruce was dissected, a much more advanced state of wood decay was observed (Laflamme, 2005). Presumably, stress created by competition in this unthinned plantation seems to be the predisposing condition to an attack by I. tomentosus. Once in the stumps, the fungus can survive more than 30 years (Lewis & Hansen, 1991). Also, in British Columbia growth reduction during at least a 40-year period has been observed (Lewis, 1997).

In short, I. tomentosus is killing groups of trees after 30 years or more of growth reduction and can cause large patches of mortality in a stand. It is present all across Canada.

Armillaria root rot

Less than 25 years ago, Armillaria root rot was said to be caused by Armillaria mellea (Vahl:Fr.) P. Kumm. Since the publication by Anderson & Ullrich (1979) recognizing 10 biological species, followed by numerous studies published by several authors, a dozen species have now been recognized in North America. The distribution of these species is better known now in Canada. Our review of the knowledge gathered (Laflamme & Guillaumin, 2005) is listed here by Canadian province (Table 1).

Table 1.  Identification of Armillaria spp. by province in Canada

Province	Armillaria spp.	Reference
British Columbia	A. ostoyae, A. sinapina, A. gallica, A. nabsnona	Morrison et al. (1985)
Alberta	A. ostoyae, A. sinapina	Mallett (1992)
Saskatchewan & Manitoba	A. ostoyae, A. sinapina, A. calvescens	Mallett (1992)
Ontario	A. ostoyae, A. gallica, A. sinapina, A. calvescens, A. mellea	Whitney (1995); Dumas (1988); McLaughlin (2001a, 2001b)
Quebec	A. ostoyae, A. gemina, A. sinapina, A. calvescens, A. mellea	Bérubé & Dessureault (1988, 1989)
New Brunswick, Nova Scotia & Prince Edward Island	Unknown
Newfoundland	A. ostoyae, A. sinapina	Bérubé (2000); (G. Warren, personal communication)

Armillaria ostoyae (Romagn.) Herink is probably the most common species found in the boreal forest, but not necessarily the most aggressive one. It seems to attack stressed trees and can kill seedlings or reduce tree growth during decades. Warren & Baines (2009) qualify this species as an aggressive opportunistic pathogen waiting for stress conditions to occur in trees. In fact, this pathogen can remain on a site in dead roots and stumps for decades as a saprophyte. Then, when tree conditions are conducive to pathogen infection, it spreads to lateral roots through subterranean rhizomorphs produced during its saprophytic phase. Later, white fungal mycelium can be observed when it becomes established in the cambium, killing the roots. This infection disturbs water and nutrient absorption by the tree which in turn affects its growth. As the pathogen progresses further into the tree, it causes root decay which often results in windthrow; trees are then uprooted or break at the base. After 20 years or more of infection, the tree will die.

In forest protection, there is a tendency to look for one pest responsible for the damage, but several factors are necessary for this root disease to occur. Using dendrochronology, Warren & Baines (2009) illustrated several cases from the simple ones to more complex situations. First, one must separate suppressed reactions in trees in the stand from root diseases. Besides suppressed trees, others can suffer the attack of one, two or more stresses impacting its growth. Different scenarios can happen: trees can recover, for example, after spruce budworm defoliation. If the impact of the stress is high then A. ostoyae can attack roots and the process is irreversible; however, the disease can go on for years without any external symptoms. Warren & Baines (2009) compared the following cases: healthy, suppressed, one impact and good recovery, one impact and poor recovery, two impacts (1989 and 1996), and three impacts (1977, 1989 and 1996). These examples should be used by dendrochronologists because they give the signature of events, not often recognized, related to root diseases.

Over time, trees can recover from several impacts. For example, in a 45-year-old red pine plantation in Arundel, Quebec, we found that the trees had been impacted up to seven times during that period including thinning and droughts (Warren & Baines, 2009). The red pines eventually died and the last pest identified was A. ostoyae. However, all the previous events recorded on growth rings are important in the history of the health state of the plantation. Tree ring patterns reflect the biotic (insects and diseases) as well as abiotic (weather) conditions during the life of a tree. Even after the death of trees, it is possible to recognize from the growth ring patterns trees that were suppressed and trees that died of root diseases (M. Cruickshank, personal communication).

Last but not least, a particular characteristic of Armillaria root diseases is the amazing size of the causal microorganism. It is the largest and oldest living organism (Smith et al., 1992). In their study, Smith et al. (1992) found an individual of A. bulbosa, now known as Armillaria gallica Marxm. & Romagn., that covers at least 15 hectares, weighs in excess of 10 000 kg, and has been genetically stable for more than 1500 years. A few years after this publication, larger specimens were found. In northeast Oregon, five genets of A. ostoyae are expanding over 20, 95, 195, 260 and 965 hectares (Ferguson et al., 2003). These Armillaria genets can continue to grow. Smaller genets can also disappear, but we do not know the reason for this yet (Guillaumin & Legrand, 2003).

Discussion

Root diseases constitute an important group of pests, if not the most destructive pests of trees in Canada (Hall & Moody, 1994). However, they do not seem to attract much attention. First, the life cycle of these pathogens can develop during several years (seven to eight years for Annosus root rot and 20–40 years for Tomentosus and Armillaria root rots) without showing any noteworthy symptoms. Second, their damages are often attributed to other causes such as windthrow, suppressed trees, insects and old age. Finally, when a root disease is diagnosed in a tree, it is too late for control intervention, the process being irreversible. Treatments for root diseases are different from the reaction mode of intervention or expensive direct control methods that are the forest protection practices commonly used in eastern Canada. We need to be proactive to control these diseases.

Root disease and silviculture

The impact of silviculture on root rots can be devastating for the forest. Intervention in a forest stand can increase the activity of root pathogens. For example, we have known since the discovery made by Rishbeth (1951) that fresh stumps created when thinning pine stands become a favourable medium for the invasion of a new site by H. annosum. The use of a preventive treatment was published about 10 years later (Rishbeth, 1963). In Canada, the oldest red pine plantations were established in Ontario. The first thinning in these plantations was done before Rishbeth's findings, which explains the invasion of this disease in eastern Canada. Later on, stump treatment with borax was used in Ontario until the late 1990s when that product was not registered for Canada any more. Despite the fact that we know the methods that can be used to prevent this very aggressive pathogen, very few actions have been taken during the last 50 years. This disease will soon reach natural jack pine stands in the province of Quebec. We observe the same attitude in Wisconsin where the disease was detected 15 years ago and no promotion for the application of preventive measures has been done since by representatives of the State. The number of infected plantations is continuously increasing in Wisconsin. On the other hand, the message from researchers to forest owners is starting to get through and we hope to have access to a commercial biological product soon to prevent further damage.

Research on Tomentosus root rot, a native disease well established throughout Canada, has provided pieces of information on the biology of the pathogen, but we do not know enough about this disease to elaborate recommendations to improve our silviculture. Prescriptions can be made in British Columbia based on soil and site characteristics (Bernier & Lewis, 1999) as well as recommendations for partial cutting (Newbery et al., 2007). In eastern Canada, site effects should be better studied to be able to draw guidelines for forest managers. The disease is very well established in the boreal forest (Lavallée, 1987). Losses can be very high in plantations. Spruce is no longer planted in the Petawawa National Forest because it will not survive more than 40 years following severe attacks by I. tomentosus (S. Deon, personal communication). The Petawawa pine sites are probably not suitable to spruce, but this has to be evaluated.

Warren & English (2003) demonstrated the negative impact of root diseases after precommercial thinning well. The intensity of thinning was too high and roots were wounded when the wind shook the trees. Several fungi classified as saprophytes in previous studies were found to be pathogens in these wounded trees.

Site preparation for reforestation can have negative effects on seedlings if Armillaria diseases are well developed on wood debris left on site. The machinery used for site preparation can spread infected material throughout the site. It may partially explain the high incidence of Armillaria disease in black spruce plantations studied in Ontario (Wiensczyk et al., 1996). Among several variables, bare root seedlings are more affected by Armillaria diseases than seedlings produced in containers (Wiensczyk et al., 1997). It is also frequent to see seedling mortality in conifers planted near hardwood stumps. The relationship between site preparation and root diseases should be better documented to be able to change practices when necessary to decrease their negative impact on seedlings. The development of biological control agents to protect seedlings against root diseases could be very innovative for successful reforestation projects on high-risk sites.

Root disease and forest entomology

Spruce infected with Tomentosus root rot seem to be colonized and killed by the spruce beetle Dendroctonus rufipenis KBY (Lewis & Lindgren, 2002). This relationship between infection by Tomentosus root rot and stresses such as drought and spruce beetle attack needs to be further studied. The case of spruce mortality at the Point Pleasant Park, Halifax, Nova Scotia is another case of a relationship between a root disease and a spruce beetle. In 1998, while participating in a NAPPO (North American Plant Protection Organisation) meeting in Halifax, I visited the park where red spruces (Picea rubens Sarg.) had died. Even though several entomologists were present, no sign of beetle presence was found, but fruiting bodies of I. tomentosus were abundant around the dead spruce which means that the pathogens could have been there for 10–20 years. It is said that the stand suffered from a severe drought in 1997 (K. Harrison, personal communication), a situation that can promote Armillaria root diseases. In 1999, an exotic insect, the brown spruce longhorn beetle (Tetropium fuscum Fabricius), was found in dying red spruces. This exotic insect had been collected in the area for 10 years before this discovery. Despite the fact that T. fuscum is recognized in Europe as a secondary insect attacking trees under stress, in Canada its status is not clear as it is said to have attacked in Point Pleasant Park trees that were ‘apparently’ healthy (http://scf.rncan.gc.ca/index/lbee), leading the reader to conclude that T. fuscum is a primary insect in Canada. We know that trees infected with Armillaria root disease can look healthy even if they are under attack by the pathogen; however, no evaluation of the disease has been conducted by researchers in this case which should have been one of the first criteria to look into.

The result of a root disease survey carried out in Manitoba spruce stands has changed the forest management plan (Knowles, 2003a). In fact, the prediction of volume losses due to Armillaria root disease was much greater than any loss attributable to a defoliator; the predicted losses increased from 14% at the time of the survey to 31% 15 years later. In another area, the volume of losses went from 8% to 25% over a 15-year span; the infested area was evaluated at 22% of the surveyed stands and the prediction for the extension of the disease reached 58% of the surface area (Knowles, 2003b). The past harvesting model based on spruce budworm damage completely changed the harvesting plan. Also, in Manitoba a pre-harvest survey of forest health conducted in 2000 showed that root disease was the most important out of the eight most common pests, with spruce budworm taking the sixth rank (Matwee, 2001). The follow-up of this survey showed that root rot diseases always ranked first with a greater percentage of importance (Matwee, 2001). Mallett & Volney (1990) proposed tree parameters to measure in mature stands. This information could indicate the cumulative effects of A. ostoyae and other stress; the hazard rating could provide a decision tool to forest managers if these stands become affected by jack pine budworm.

In old spruce plantations located in the Mauricie region, north of Trois-Rivières, Quebec spruce have been known to be severely affected by I. tomentosus and Armillaria root diseases for 40 years (Ouellette, 1967). Mortality occurred recently and it was attributed to spruce budworm defoliation. No observation in dendrochronology was performed on these trees, but the dead trees were not drying and standing; they were falling in all directions soon after dying which is a good indication of root disease. It is quite possible that the defoliation was the last impact that accelerated the mortality of these moribund spruces. A similar case was observed in a spruce plantation owned by Hydro-Quebec near Drummondville, Quebec. That plantation was known to be severely damaged by Armillaria root disease (B. Boulet, personal communication) and it was even possible to see the loss of older needles in reaction to the disease, but again defoliation by spruce budworm in the plantation was said to be the cause of spruce mortality.

Root disease and forest ecology

Forest ecologists define ecosystemic forest management as follows:

‘A management approach that aims to maintain healthy and resilient forest ecosystems by focusing on a reduction of differences between natural and managed landscapes to ensure long-term maintenance of ecosystem functions and thereby retain the social and economic benefits they provide to society’ (Gauthier et al., 2009).

Root diseases are included in this definition, but seem to be excluded by ecologists. Only forest fire, spruce budworm and forest tent caterpillar (Malacosoma disstria HBN.) are retained as main disturbance factors having an impact on forest dynamics in the boreal forest (Vaillancourt et al., 2009a). Windthrow is also often cited (Jetté et al., 2009). Root diseases, which have a major impact on wood losses, seem to be eliminated because of the apparently small area affected for a given event and the long period of time, i.e. the several decades it takes for root diseases to cause visible damage (Vaillancourt et al., 2009b). It is evident that these three selected agents are easily detectable, that they cover a large area in a given space, and that their related damages are done over a short period of time. All these conditions make it easier to measure the area of forest affected. With root rot diseases, on the other hand, total affected areas calculated by the addition of thousands of infection centres in the boreal forest is certainly greater than total defoliated area, but it is not quite visible in a given space and in a short time period. Nevertheless, while root diseases do not seem to change the landscape, the losses in volume they cause make them one of the most important forest pests. They are active year after year, not confined to a given age class, and are active all over the forest.

On the other hand, forest ecologists indirectly recognize the impact of root rot, but they attribute stand gaps in the boreal forest to other causes such as spruce budworm and windthrow (D'Aoust et al., 2004; Pham et al., 2004). The description of these gaps corresponds to root disease centres which are part of the forest ecosystems (Morrison & Mallett, 1996). Our hypothesis is that when defoliators hit a stand, trees with root rot will be killed first, or if a stand is hit by strong winds, trees with root rot will be the first to fall over. When looking at a forest ecosystem, we shall not try to oversimplify the natural process, but keep in mind the ‘cascade of events’ that may have led to a particular situation.

Finally, it is often believed that mortality in younger stands is caused by suppression, but root diseases are involved at any stage in the stand, from seedlings to very old trees. Therefore, we shall not consider root diseases only as a normal process of ageing trees: a 40-year-old spruce is not an old tree in the boreal forest. This type of tree mortality caused by Armillaria root diseases has been observed in forest stands at all ages by looking at the dendrochronology of recently dead trees (M. Cruickshank, personal communication).

Conclusion

With the exception of exotic pathogens, diseases are an important component of our forest ecosystems and we have to understand their role to optimize the productivity of this renewable natural resource. Losses attributable to root diseases are probably more harmful than those caused by any other pests and they are present in all forest stands of all ages across Canada causing different levels of damage.

Being less visible, root diseases do not receive much attention in spite of their importance. Statistical reports on forest pests give information on damage occurring over a 1-year period, eliminating ipso facto information on root diseases. Root diseases usually develop over a long period of time, up to several decades, on trees that do not show conspicuous symptoms. It is a good reason to make more risk assessment of root diseases to quantify their impact, like the one done in British Columbia on A. ostoyae (Cruickshank, 2009).

There are indications that the impact of root diseases will continue to increase. Even aggressive fungal pathogens like H. annosum have received little attention despite the fact that this disease is about to invade British Columbia on the west coast and jack pine stands in eastern Canada. Following precommercial thinning operations carried out in Newfoundland, root rot has done considerable damage to residual trees and a change in microbial diversity has also been noted; fungi that were seldom found in natural stands have become more frequent (Warren & English, 2003). Younger, successful conifer plantations suffer from root diseases when they reach the age of 30–40 and the conditions leading to this situation are unknown.

There is a need for research on root diseases. Because of the difficulty in seeing these diseases, priority should be given to detection methods. Dendrochronology should be better documented for different stress factors including root diseases (Mallett & Volney, 1999; Warren & Baines, 2009). The possibility of using instruments like a resistograph to detect root diseases in trees should be investigated. Large-scale aerial photography should be developed specifically to detect infection circles as in the trials conducted in Manitoba (Knowles, 2003b). More mapping procedures should be developed to better assess root diseases at an operational level (Reich, 2009). The impact on conifer regeneration of natural populations of Armillaria root disease developing on hardwood stumps should be better quantified. The relationship between site preparation and Armillaria root diseases should be better understood and biological control agents should be developed to decrease the impact of root diseases. The list could go on.

The most important factor overall is a better integration of the work done by different specialists interested in forest protection. Forest pathologists have been used to include numerous factors in their studies, including abiotic ones as well as insects and pathogens, especially when working with tree dieback or decline. Forest entomologists, forest ecologists and professional foresters should focus more on the forest ecosystem including all important elements of the ecosystem. When one of the greatest living organisms is left out of the ecosystem, such as is the case with Armillaria individuals being able to cover hundreds of hectares, we have to conclude that this ecosystem is truncated. A solution for a better integration would be to bring back mandatory courses in forest pathology and forest entomology in Canadian universities that offer forestry programmes. A better solution would be to develop a course integrating all biotic and abiotic factors in forests, as that presented in the book by Schwerdtfeger (1981) in Germany. Unfortunately, we do not have any equivalence in North America.

Notes

^†Contribution to the symposium “Root Diseases; Challenges and Perspectives” held during the Canadian Phytopathological Society Annual Meeting, 22–25 June 2009, Winnipeg, MB.