The spreading of the S type of Heterobasidion annosum from Norway spruce stumps to the subsequent tree stand

The occurrence of Heterobasidion annosum in stumps and growing trees was investigated on 15 forest sites in southern Finland where the previous tree stand had been Norway spruce (Picea abies) infected by H. annosum, and the present stand was either Scots pine (Pinus sylvestris), lodgepole pine (Pinus contorta), Siberian larch (Larix siberica), silver birch (Betula pendula) or Norway spruce 8–53 years old. Out of 712 spruce stumps investigated of the previous tree stand, 26.3% were infected by the S group and 0.3% by the P group of H. annosum. The fungus was alive and the fruit bodies were active even in stumps cut 46 years ago. In the subsequent stand, the proportion of trees with root rot increased in spruce stands and decreased in stands of other tree species. On average, one S type genet spreading from an old spruce stump had infected 3.0 trees in the following spruce stand, 0.5 trees in lodgepole pine, 0.3 trees in Siberian larch, 0.05 trees in Scots pine and 0.03 trees in silver birch stand. Although silver birch generally was highly resistant to the S type of H. annosum, infected trees were found on one site that was planted with birch of a very northern provenance.     

Transfer of the P-type of Heterobasidion annosum from old-growth stumps of Picea abies to Picea abies and Larix×eurolepis

The infection of Picea abies and Larix x eurolepis by Heterobasidion annosum was studied in felled trees in Sweden. Thinnings were carried out in two stands of L. x eurolepis, 15 and 20 years old, and in a 25-year-old stand of P. abies, established on a site heavily infected by H. annosum. The 15- and 20-year-old L. x eurolepis stands exhibited the greatest incidence of butt rot with infections amounting to 38 and 57%, respectively, of removed trees. The incidence of butt rot in the P. abies stand was only 5%. Heterobasidion annosum was the main butt rot causing fungus. All isolates of H. annosum were of the P-intersterility group. Transfer of H. annosum from old-growth P. abies stumps to trees felled in the thinning of the next generation was demonstrated by somatic incompatibility tests. However, the majority of infections could not be connected with decay already established in the previous generation. In L. c eurolepis, rot columns were frequent, including also several genotypes in the same stem, and typically positioned in the inner sapwood. The few infections of P. abies were situated in the heartwood.     

Optimizing the management of a Picea abies stand under risk of butt rot

A simulation model was developed to predict the growth of a Norway spruce stand under risk of butt rot caused by Heterobasidion annosum stump infection and logging injuries. The simulation model was distance‐dependent; tree growth was predicted with a distance‐dependent model, and the spread of butt rot through root contacts depended on tree location. Infection of stumps and injured trees, and the spread of butt rot in the stand were stochastic processes whereas tree growth and mortality were treated as deterministic processes. The simulation model was used with the nonlinear optimization algorithm of ooke and J eeves (J. Assoc. Comput. Mach, 8, 212–229, 1961) to find the most profitable management schedule for an even‐aged, young stand. Optimization used four different stump infection rates and two spreading capacities from infected stumps. The profitability was evaluated by the expected soil expectation value (SEV) at a 3% interest rate. Two thinnings, both in winter‐time, and hence without H. annosum infections, resulted in the highest SEV. If any stump infection by H. annosum occurred, only one thinning and a shortened rotation were suggested. The optimal thinning rate tended to decrease but also large trees were removed with the increasing infection rate. With one thinning during a rotation, stump treatment was profitable above a stump infection rate of 10%     

Serpula himantioides,Heterobasidion annosum and Calocera viscosa as butt rot fungi in a Danish Douglas‐fir stand

A scattered wind fall of 50 trees in a 46‐year‐old stand of Douglas‐fir (Pseudotsuga menziesii) revealed Serpula himantioides, Heterobasidion annosum and Calocera viscosa as decay causing fungi. Sixty‐four percent of the stumps had visible rot on the stump surface. Mainly, a central brown rot was seen, caused by either S. himantioides or C. viscosa combined with eccentrically placed spots of incipient H. annosum rot. Subsequently, the appearance of fruitbodies disclosed that in total 76% of the wind thrown trees were associated with one or more of the three decay fungi. S. himantioides was present in a surprisingly large number of trees (54%), and the rot column extended up to 2 m into the stem. This investigation represents the first known incidence of S. himantioides and C. viscosa causing root and butt rot in living conifers in Denmark.     

Effectiveness of treatment of Norway spruce stumps with Phlebiopsis gigantea at different rates of coverage for the control of Heterobasidion

The natural establishment of the root and butt rot causing fungus Heterobasidion annosum s.l. on Norway spruce (Picea abies) thinning stumps treated with Phlebiopsis gigantea was investigated on seven sites in southern Sweden. The trees were cut during summertime and the stumps were treated with different patterns simulating the effect of mechanical stump treatment with a single‐grip harvester. Sampling was conducted 3 and 12 months after treatment. At both samplings, the best control was obtained when 100% of the stump surface was covered by P. gigantea: in contrast, untreated control stumps showed the highest incidences of H. annosum s.l. infection at both sampling times. However, 30 and 26% of the fully covered stumps at the first and second samplings, respectively, were diseased, and question the efficacy of treating Norway spruce stumps with this biological control agent in Sweden.     

Hosts and distribution of the intersterility groups of Heterobasidion annosum in the highlands of Greece

The intersterility groups of 127 pure cultures of H, annosum collected from different host trees in 12 mountain areas in Greece were identified. The F group commonly caused butt rot on the fir species Abies cephalonica and Abies borisii regis. It was the only type of H. annosum found in pure fir forests. The P group caused serious root rot in pinus sylvestris stands in north-eastern Greece. In more southern mountain areas it often colonized stumps of pinus nigra but seldom killed this tree species. The S group was found in natural forests of Picea abies in northern Greece, causing butt rot of spruce. In mixed forests, the intersterility groups of H. annosum were found relatively often in stumps of tree species other than their main hosts, although some host preference seemed to occur also in stump colonization.     

Root and butt rot of Todo fir (Abies sachalinensis) caused by Heterobasidion annosum s.l. in Hokkaido,Japan

The occurrence and symptoms of root and butt rot were examined in a 35 × 30 m plot of 68‐year‐old Todo fir plantation in Hokkaido, Japan. Forty‐seven percent of the cut stumps were decayed and 52% of the decayed stumps showed similar decay characteristics with yellowish orange to light brown colouration and expanded pockets in the heartwood. Morphological characteristics of the pure cultures isolated from the decay were similar to the cultures isolated from basidiocarps of Heterobasidion annosum sensu lato, found on fallen logs outside of the research site. Also DNA analysis based on the combined data set of three gene loci (glyceraldehyde 3‐phosphate dehydrogenase, heat shock protein 80–1 and elongation factor 1‐alpha genes) showed that the isolates from the decay are included in the same clade with the Japanese H. annosum s.l. isolates. They form a subclade to H. parviporum (the European S group of H. annosum s.l.). This is the first report of molecular determination of H. annosum s.l. isolated from root and butt rot in a plantation in Japan.     

Intraspecific variation in Heterobasidion annosum for growth in sapwood of Picea abies and Pinus sylvestris

Two greenhouse experiments were conducted to study intraspecific variation in growth of the root rot fungus Heterobasidion annosum in living host sapwood. In experiment 1, Scots pine (Pinus sylvestris) and Norway spruce (Picea abies) seedlings were inoculated with H. annosum isolates, 14 each of the S-and P-intersterility groups, collected from various parts of Sweden. In pine, the P-group isolates were more virulent than the S-group isolates both in terms of infection frequency, induced mortality rate (p < 0.05), and fungal growth in sapwood (p < 0.05). In spruce, the P-group isolates were also more virulent on average, but the difference was not statistically significant. Both S and P isolates had a higher infection frequency and a significantly longer sapwood growth on spruce than on pine. The P-group caused higher mortality on pine than on spruce. The length of the lesion in the inner bark was strongly correlated with fungal growth in spruce, but not in pine where the lesions were short or absent. In experiment 2, ten Norway spruce clones were inoculated with 18 S-isolates, originating from nine live-decayed trees and from nine spore-infected stumps in a single Norway spruce stand. The objective was to test whether any selection for growth rate in sapwood was detectable among individuals of H. annosum originating either from stumps or trees. The results gave no support for such selection since no difference in sapwood growth between the two groups of isolates was found.     

Controlling and predicting the spread of heterobasidion annosum from infected stumps and trees of picea abies

Two Norway spruce stands with heavy infections of Heterobasidion annosum were clear‐cut in 1957 and 1959 in Sweden. The stumps were extracted, the soil sifted to remove most of the roots, and young Norway spruce were planted. After 25 and 28 years, H. annosum had infected 1 % and 2% of trees on plots where stumps had been removed and 17 % and 12% of the trees on control plots, respectively. Several of the H. annosum clones fruiting on old‐growth stumps were also detected in decayed, standing trees. The same fungal clone was found to be infecting adjacent trees from several old‐growth stumps. In addition to old stumps, stumps from recent thinnings and diseased living trees were traced as infection sources. Their relative importance in spreading disease was estimated. Disease risk predictions based on the distance of a tree from various infection sources correlated well with observed frequencies of rot.     

Incidence of Heterobasidion annosum in precommercial thinning stumps in coastal British Columbia

Coniferous stumps in 83 stands in coastal British Columbia were sampled 3-5 years after precommercial thinning. The percentage of stumps and surface area colonized by Heterobasidion annosum were determined for 25 stumps of each species in each 5-cm diameter class present in each stand. There were significant differences among species in the percentages of stumps and surface area colonized, with Douglas-fir (Pseudotsuga menziesii) having the lowest values, amabilis fir (Abies amabilis) and Sitka spruce (Picea sitchensis) the highest and western hemlock (Tsuga heterophylla) being intermediate. For stumps of each species 5–20 cm in diameter, both the percentage of stumps and surface area colonized increased with increasing diameter. In stumps that were grafted to an adjacent tree, there was decreased incidence of H. annosum for Douglas-fir and Sitka spruce and increased incidence for western hemlock and amabilis fir. There were trends in the percentage of stumps and area colonized for season of thinning and biogeoclimatic subzones with the values for most species decreasing as the amount of precipitation increased. Colonization of precommercial thinning stumps by H. annosum occurs throughout the coastal region of British Columbia, and this will increase the amount of inoculum and will likely increase the incidence of butt rot. The results of this study suggest that the increase in inoculum can be minimized by thinning before age 15, by cutting only trees less than 10 cm in diameter and by thinning during low risk seasons.     

Distribution of Heterobasidion annosum intersterility groups in Poland

Specimens of Heterobasidion annosum were collected in 104 different stands in 43 regions of Poland. Pure cultures originating from 439 collections were identified in mating tests. Three intersterility groups, P, S and F, of H. annosum were found. Their occurrence in Poland was connected with the natural distribution of the main hosts: Pinus sylvestris, Picea abies and Abies alba, respectively. P was the most common intersterility group of H. annosum in Poland, causing mortality in Scots pine plantations and root rot in older stands. It was also isolated from Betula pendula, P. abies, Larix decidua, Fagus sylvatica and Carpinus betulus. The S group was present in the southern and north‐eastern parts of the country, causing root and butt rot mostly in spruce stands. The F group occurred in the south of Poland, in the mountains, highlands and lowland up to the northern border of the distribution of fir. It was found only on stumps, old dead trees and logs. There was no evidence of damage caused by the F group on A. alba trees.     

Early infection of Fagus sylvatica by Heterobasidion annosum sensu stricto

Heterobasidion annosum sensu stricto is the most important damaging agent in Scots pine stands planted on the former agricultural lands in Poland. The routine action in pine stands which have lost stability because of H. annosum root rot is to change stand management, including species conversion. In many cases, the Fagus sylvatica is used for this purpose. This study was the first assessment of widespread infection by H. annosum in young F. sylvatica plantations. Disease symptoms included atrophy and yellowing of leaves, wilting and the presence of pathogen sporocarps around the root collars of young trees. Heterobasidion annosum s. s. was observed on both 4‐ and 17‐year‐old beech. Based on annual increments, the disease could be present for 3–4 years before tree death. A high incidence of H. annosum in pine stumps of previous stands (80–100%) and dry periods in recent years may be the main reasons for such common infection of F. sylvatica. This work also showed that mice and frost were not the main killing factors F. sylvatica in plantations.     

Epidemiology of Heterobasidion abietinum and Viscum album on silver fir (Abies alba) stands of the Pyrenees

In the last two decades, stand decline and increased mortality has affected silver fir (Abies alba) forests in the Spanish Pyrenees. Simultaneously severe occurrences of the root rot fungus Heterobasidion annosum s.l. and of the mistletoe Viscum album have been reported. We aimed to improve the understanding of the epidemiology of both pathogens in our region. All H. annosum isolates found on silver fir were typed as H. abietinum. H. abietinum was more frequently observed where cuttings had targeted fir trees rather than other species. H. abietinum fruiting bodies were observed in the most recently cut stumps. V. album was more abundant on more dominant fir trees, and in southern aspect stands. The number of V. album colonies in the stand correlated (R² = 0.40) with silver fir mortality. Stands with a high level of V. album infection tended to have a smaller percentage of basal area in species other than silver fir, and they tended to be located on more south‐facing slopes. H. abietinum was widespread in silver fir forests of the Pyrenees. Our data suggest that, in the Pyrenees, the observed H. abietinum incidence may represent a combination of both primary and secondary spread of the pathogen. Favouring mixed forests should be tested as a potential control method for V. album. The correlation between silver fir mortality and V. album infection warrants further study, as the observed tree mortality could have occurred due to other factors than V. album, such as drought damage.     

Untersuchungen zur biologischen Bekämpfung von Heterobasidion annosum an Fichte (Picea abies) mit antagonistischen Pilzen II. Interaktionstests auf Holz

Investigations on biological control of Heterobasidion annosum in Norway spruce with antagonistic fungi. II. Interaction experiments in wood . Seventeen fungal species were examined for antagonism against H. annosum in wood. After inoculation of stem sections and stumps by conidia and dowels, the distribution patterns of the mycelia within the wood were recorded. In spruce-wood antagonism was shown only by Hypholoma capnoides, Bjcrkandera adusta, Resinicium bicolor and Trichoderma spp. near the site of inoculation. As the distance from this site increased H. annosum became more dominant. Inoculations by dowels yielded more infections than inoculations by spores. The patterns of myeelial distribution within the wood were similar in stem sections and in stumps. Spruce stumps were colonized naturally mainly by Resinicium bicolor, Armillaria mellea s. I. and Nectria fuckeliana. In stem sections of Pinus sylvestris, however, Phlebiopsis gigantea displaced H. annosum effectively.     

Resinicium bicolor; a potential biological control agent for Heterobasidion annosum

After introductory competition tests in the laboratory, Resinicium bicolor was used as a potential control agent for the conifer root rot fungus Heterobasidion annosum. Greenhouse pathogenicity tests with R. bicolor on 4-year-old seedlings of Norway spruce (Picea abies) and Scots pine (Pinus sylvestris) showed moderate incidence of infection. In three places in Sweden, four test areas were chosen for field experiments in first-rotation plantations and also in old forest sites of Norway spruce. Wood blocks, pre-inoculated with one strain of R. bicolor, were buried in the soil beside stumps at 0, 1, 2, 3 and 4 months after thinning using various spatial designs. In two of the test areas, half of the stumps were treated with a suspension of H. annosum conidia from one strain by surface spraying. After 2–3 years, stump roots were investigated and the length of growth of both species were noted. The identity of mycelia reisolated from and wood debris in the test areas were confirmed by somatic compatibility tests with the original strains. The strain of R. bicolor released was recovered from all over the test area; the released H. annosum strain was only reisolated from the conidia sprayed stump roots. R. bicolor had little effect on the growth and occurrence of H. annosum. Potential control of disease spread may arise, however, from occlusion of the pathogen from outer parts of roots.     

Higher resistance of the offspring of Scots pine trees resulting from natural regeneration in old foci of Heterobasidion annosum root rot

Abstract

Heterobasidion annosum (Fr.) Bref. is a fungal pathogen causing annosum root rot – one of the most economically important diseases in coniferous stands. The major aim of this study was to compare the resistance of the offspring of Scots pine trees (Pinus sylvestris L.) from seed orchards and the offspring of trees that were naturally reproduced in old foci of the disease. In experiments conducted in vitro, we used 960 seedlings which were grown from seeds collected from 60 trees in 6 old foci of the disease and 640 seedlings grown from seeds collected in 4 seed orchards. The offspring of trees from seed orchards after inoculation with H. annosum had nearly twofold higher mortality rate than the seedlings developed from the seeds collected in old foci of the disease. This suggests that the offspring of self-sown trees in old foci of the disease has a greater, genetically conditioned resistance to annosum root rot.     

Urea treatment reduced Heterobasidion annosum s.l. root rot in Picea abies after 15 years

Stump protection using chemical or biological agents is the main control measure against root and butt rot caused by Heterobasidion annosum s.l. in northern and temperate conifer forests. Long-term effects of urea treatment of stumps are poorly known and here we describe a 15-year study of urea treatment on the rot incidence on Norway spruce (Picea abies). We also tested the effect of urea protection on tree growth and on the resistance of stands against strong winds. Four treatments were made in two replications in two first-rotation P. abies stands in southern Sweden; after first-thinning stumps were (i) treated with urea 35% (w/v), (ii) artificially infected with H. annosum conidia, (iii) half urea treated and half artificially conidia infected, (iv) untreated, therefore naturally infected. After 15 years, the trees were sampled at 20 cm above ground using an increment borer and observed for presence of rot and, following incubation, presence of H. annosum conidia. Tree growth was calculated by measuring the diameter before and after the treatment. Urea treated plots showed the lowest incidence of rot (3%) as well as of H. annosum incidence (0%). Conidia treatment showed the highest incidence of rot (68%), its incidence was higher than that observed in natural infection treatment (43%), but did not differ from that of the 50% conidia treatment (47%). On about 30% of the rotted trees we observed conspicuous H. annosum fruiting. We did not observe growth reduction associated with tree rot. H. annosum was the only fungus observed associated with rotted trees which suggest that it was responsible for most of the rot observed in the investigated plots. Urea treated plots showed the lowest incidence of windthrown trees, and 59% of the windthrown tree incidence among the plots was explained by the incidence of H. annosum. Urea can be regarded as a reliable long-term protection method against root and butt rot of Norway spruce.     

In vitro interactions between bacteria isolated from Sitka spruce stumps and Heterobasidion annosum

Culture medium composition affected antagonism by bacterial isolates from Sitka spruce (Picea sitchensis) stumps against Heterobasidion annosum. Fifty percent of bacterial isolates inhibited H. annosum growth on sporulation agar or yeast–dextrose–peptone agar; only 10% of isolates caused inhibition on both media. Proportions of isolates inhibiting H. annosum varied with stump age; fewer isolates from 4‐ or 6‐year‐old stumps exhibited antagonism than isolates from older or younger stumps. Fifteen isolates showing antagonism on sporulation agar were tested against H. annosum in spruce wood cubes. None of the bacterial isolates alone caused a significant weight reduction in inoculated cubes. Relative inoculation times of bacterial isolates and H. annosum had an effect on weight loss in interactions; simultaneous inoculation with isolates and H. annosum inhibited weight loss caused by H. annosum compared with bacteria‐free controls. Inoculation with bacterial isolates 10 days before H. annosum had no effect on the decay rate. In contrast, inoculation with H. annosum 10 days before bacteria increased weight loss of cubes by 200% relative to cultures lacking bacteria. The effect of a mixed bacterial inoculum on weight change in 0.2‐mm spruce wood slips co‐inoculated with H. annosum, Resinicium bicolor, Hypholoma fasciculare, Stereum sanguinolentum or Melanotus proteus differed between different fungi.     

Reaction zone and periodic increment decrease in Picea abies trees infected by Heterobasidion annosum s.l.

Norway spruce (Picea abies) trees infected by Heterobasidion annosum s.l. decrease their periodic increment after a long period of time. Periodic increment decrease hypothetically relates to the formation of a reaction zone in order to prevent fungal colonisation. We studied 11 stands in Sweden, where we compared the periodic increment of healthy, rotten- and H. annosum-infected trees growing on plots thinned in winter, unthinned or thinned in summer, with and without urea or P. gigantea treatment of the stumps. Based on the rot incidence and the population structure of H. annosum of the plots, two phases of infection were considered: > 13 years and < 13 years. The presence of reaction zone and decay was observed on wood cores extracted with an increment borer. Rotten and H. annosum-infected trees with reaction zones exhibited a lower periodic increment than healthy trees (13.0% and 12.5% losses in terms of diameter, respectively), while no differences were observed between healthy trees and rotten and H. annosum-infected trees without reaction zone. Our results support the hypothesis of a periodic increment decrease in individual trees due to photosynthate re-allocation resulting from decay compartmentalization. Periodic increment decrease was only evident in trees that had been infected for more than 13 years. Trees in urea-treated plots registered a higher periodic increment, suggesting a possible response of trees to the nitrogen addition of the urea treatment of the stumps.     

Swiss stone pine trees and spruce stumps represent an important habitat for Heterobasidion spp. in subalpine forests

In the Western Italian Alps (WIA), the three European species of the forest pathogen Heterobasidion spp. can coexist in the same area. Heterobasidion parviporum Niemelä & Korhonen and Heterobasidion abietinum Niemelä & Korhonen are normally found in areas with a significant presence of their respective primary hosts, spruce (Picea spp.) and fir (Abies spp.). The host/niche occupied by Heterobasidion annosum (Fr.) Bref. in the region still remains unclear. Although Scots pine (Pinus sylvestris), a major host for this fungal species in other parts of Europe, is abundant in the region, little or no evidence of disease caused by H. annosum is visible in this tree species. Two different, but not mutually exclusive, hypotheses can explain the presence of H. annosum: (1) Scots pines are infected but largely asymptomatic and (2) H. annosum has adapted to different hosts. An analysis of Heterobasidion species was performed in two natural, mixed‐conifer forests using traditional isolation techniques and novel direct molecular diagnosis from wood. In a subalpine stand of mixed spruce (Picea abies), larch (Larix spp.), and Swiss stone pine (Pinus cembra), 18 naturally infected spruces and larches only yielded H. parviporum. A Swiss stone pine in the same stand was extensively colonized by both H. parviporum and H. annosum. In a second subalpine stand, an analysis of 18 spruce stumps and nine Swiss stone pine stumps yielded both H. parviporum and H. annosum isolates. Pine stumps had been mostly colonized by H. parviporum prior to tree felling, suggesting that this species may be secondarily infected by the locally predominant Heterobasidion species (i.e. H. parviporum). Results of our analysis also indicated that primary colonization of spruce stumps (e.g. through basidiospores) was caused by both H. parviporum and H. annosum, while secondary infection of such stumps was mostly because of H. parviporum.