Next Article in Journal
Evaluation of the Impact of Timber Truck Configuration and Tare Weight on Payload Efficiency: An Australian Case Study
Next Article in Special Issue
Molecular-Based Reappraisal of a Historical Record of Dothistroma Needle Blight in the Centre of the Mediterranean Region
Previous Article in Journal
Suppressed Undergrowth of Siberian Spruce (Picea obovata Ledeb.) in Early Ontogeny: One-Way Ticket or Survival Strategy?
Previous Article in Special Issue
Gypsy Moth Management with LdMNPV Baculovirus in Cork Oak Forest
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 12
Issue 7
10.3390/f12070854
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Inferences on the Susceptibility of Wood of Different Tree Species to Heterobasidion annosum Sensu Lato Primary Infections and on the Range of Pathogen Spores Dispersal

by
Lauma Brūna
1,*,
Guglielmo Lione
2,
Kristīne Kenigsvalde
1,
Natālija Burņeviča
1,
Astra Zaļuma
1,
Dārta Kļaviņa
1,
Tālis Gaitnieks
1 and
Paolo Gonthier
2
1
Latvian State Forest Research Institute Silava, 111 Rigas Street, LV-2169 Salaspils, Latvia
2
Department of Agricultural, Forest and Food Sciences (DISAFA), University of Turin, Largo Paolo Braccini 2, 10095 Grugliasco, Italy
*
Author to whom correspondence should be addressed.
Forests 2021, 12(7), 854; https://doi.org/10.3390/f12070854
Submission received: 24 May 2021 / Revised: 14 June 2021 / Accepted: 24 June 2021 / Published: 28 June 2021
(This article belongs to the Special Issue Forest Pathology and Entomology)
Browse Figures
Versions Notes

Abstract

:
Stumps play a pivotal role in the epidemiology of the fungal forest pathogens Heterobasidion spp. because they are the main courts of primary airborne infections. The aims of this study were (i) to determine the susceptibility of seven tree species (i.e., Larix sibirica, Picea abies, Picea sitchensis, Pinus contorta, Pinus strobus, Pinus sylvestris and Pseudotsuga menziesii) to primary infection by H. annosum and H. parviporum through comparative inoculation experiments of conidia on wood discs in controlled conditions; (ii) to compare the susceptibility of wood discs of the same tree species to natural airborne infections in two Latvian Norway spruce forest stands infested either by H. annosum or H. parviporum; (iii) to explore the rates of infection of wood discs at increasing distances from spore sources in these two forests to make inferences on the range of spores dispersal. Results obtained by spraying wood discs with conidial suspensions in controlled conditions are in agreement with those obtained by exposing wood discs to the natural airborne inoculum in the forests, as clearly supported by the significant correlation (r = 0.79; p < 0.05) between the two sets of data. Susceptibility was highest in Pinus species, followed by P. abies and P. sitchensis. Susceptibility was lowest for L. sibirica and P. menziesii. The area colonized by Heterobasidion spp. in the sapwood of wood discs was much greater than that colonized in the heartwood. A sharp decrease in the rate of infection of wood discs with distance from spore sources (i.e., fruiting bodies) was observed, further confirming the importance of local spore sources in the epidemiology of Heterobasidion spp. Taken together, these findings could help designing tactics to manage these fungal forest pathogens.

1. Introduction

Heterobasidion is a genus of basidiomycetes in the family of Bondarzewiaceae, including several species, two of which, i.e., H. annosum (Fr.) Bref. and H. insulare (Murrill) Ryvarden, have been reported to be species complexes [1]. While most Heterobasidion are saprotrophs, those included in the H. annosum species complex, hereafter referred to as H. annosum sensu lato (s.l.), are pathogenic and may be particularly damaging, especially in managed coniferous stands [1,2]. Within H. annosum s.l., three native species occur in Europe: H. abietinum, H. annosum sensu stricto (s.s.), hereafter referred to as H. annosum, and H. parviporum. While the former is found mainly in central and southern Europe in association with its main host, silver fir (Abies alba Mill.), H. annosum and H. parviporum are more widespread throughout Europe, including the Baltic States [2,3,4]. Heterobasidion annosum and H. parviporum display different host preferences: H. parviporum mainly infects Norway spruce (Picea abies (L.) H. Karst.), whereas H. annosum is commonly associated with pines (Pinus spp.), especially Scots pine (Pinus sylvestris L.), although it can also infect Norway spruce and some deciduous trees [5,6,7]. In addition, the North American invasive H. irregulare has been reported in Italy on Italian stone pine (Pinus pinea L.) [8,9,10].
Heterobasidion annosum s.l. spreads by means of spores infecting either freshly cut stump surfaces or trees through tree wounds [1]. Once the fungus has colonized the root systems of stumps or trees, it can spread to neighboring healthy trees by the propagation of the mycelium, provided that root contacts are present [1]. Infection through spores and by the propagation of the mycelium are known as primary and secondary infections, respectively. Primary infection is mainly caused by basidiospores (sexual spores), which are produced in large amounts by fruiting bodies. The fungus also produces conidia (asexual spores), although the role of conidia in the infection process in nature seems to be negligible [11].
The susceptibility of different tree species to species of H. annosum s.l. has been extensively analyzed by determining the disease incidence in secondarily infected trees in naturally infested stands [12,13,14,15,16,17]. On the contrary, the susceptibility of stumps of different species to primary infection by H. annosum s.l. has received much less attention, and only a few studies have been conducted on this topic. In the Alps, Norway spruce was reported as significantly more susceptible to airborne stump infection by H. annosum s.l. than European larch (Larix decidua Mill.), silver fir and Scots pine, in that order [18]. Studies carried out in Latvia also showed that Norway spruce stumps are more susceptible to H. annosum s.l. airborne infection compared to Scots pine stumps [19].
As previously postulated [18], the comparison of levels of susceptibility of stumps of different tree species to primary infection by H. annosum s.l. is complicated by the fact that such analyses would require stumps of different species to co-occur in the same forests, which is not always the case. However, referring to H. annosum s.l., epidemiological traits related to spore release and deposition have been successfully revealed by exposing in the forest wood discs of conifers simulating stumps [17,18,20,21,22,23,24,25,26]. For those purposes, wood discs of Norway spruce, less often Scots pine, silver fir and larch have been employed. In addition, wood discs of Norway spruce, Italian stone pine and silver fir have been recently and successfully used to test the efficacy of biological and chemical treatments against species of H. annosum s.l. [27]. Only a few studies explored the susceptibility to artificial or natural spore infection by H. annosum s.l. of wood discs of different tree species at the same time. Redfern [28] analyzed the germination of H. annosum basidiospores inoculated on stem sections of Scots pine, lodgepole pine (Pinus contorta Douglas) and Sitka spruce (Picea sitchensis (Bong.) Carr.), whereas Thomsen and Jacobsen [29] investigated the growth of formerly inoculated H. annosum mycelium in discs of Norway spruce, Scots pine, hybrid larch (Larix × eurolepis Henry), Sitka spruce, and Douglas fir (Pseudotsuga menziesii (Mirbel) Franco). Dimitri et al. [30] determined the number of H. annosum s.l. spores deposited on P. abies and P. sylvestris wood discs exposed in Norway spruce stands, while Wang et al. [26] made the same by exposing wood discs of Larix × eurolepis, P. abies and P. sylvestris in hybrid larch stands. To date, no studies have compared the levels of susceptibility of wood discs of different tree species to the infection by spores or conidia of H. annosum s.l. using wood discs originating from the same trees.
All the analyses on the susceptibility of stumps to airborne infections by H. annosum s.l. have been made by considering the species complex level; therefore, there is little knowledge on whether the susceptibility of stumps of different tree species may differ depending on the Heterobasidion species involved, as previously postulated [18]. The assessment of the risk of primary infection by H. annosum s.l. would be particularly important to predict the likelihood of establishment of the pathogen but also to modulate the intensity of thinnings on a given tree species in order to minimize the risk of outbreaks.
In Latvia, forests occupy 52% of the country’s territory, and the area covered by Norway spruce and Scots pine is 46% of the total forest area [31], which underlines the importance of these dominant tree species in Latvian forestry. However, in the context of climate change, the proportion of other non-native conifer tree species may increase [32], requiring investigation of their susceptibility to native H. annosum s.l. species, i.e., H. annosum and H. parviporum.
Primary infection by H. annosum s.l. on stumps depends on the levels of spore loads, which have been reported to vary depending on the season and on the distance from spore sources (i.e., fruiting bodies) [1]. Studies conducted in Sweden showed that spore deposition rate and the risk of stump infection reach a maximum in May to August [33], while in the Alps, spore deposition rate and risk of stump infection peak at the end of summer and autumn [18,24]. Most of H. annosum s.l. spores land within a few meters from fruiting bodies, and only a minority can travel 100 m and further [34,35]. Other studies indicate that a considerable amount of spores can spread 100 m from spore sources [21,36]. Most of the information on the range of spore dispersal of H. annosum s.l. refers to Norway spruce stands of Northern Europe [21,25] or to mixed oak–Italian stone pine stands of the Mediterranean Region [36]. There is a complete lack of knowledge on the levels of spore loads and on the range of spore dispersal in Norway spruce stands of the Baltic Region.
The aims of this work were (i) to determine the susceptibility of seven tree species to primary infection by H. annosum and H. parviporum through comparative inoculation experiments of conidia on wood discs in controlled conditions; (ii) to compare the susceptibility of wood discs of the same tree species to natural airborne infection in two Latvian Norway spruce forest stands infested either by H. annosum or H. parviporum; (iii) to explore the rates of infection of wood discs at increasing distances from spore sources in these two forests to make inferences on the range of spore dispersal.

2. Materials and Methods

2.1. Comparative Susceptibility of Wood Discs of Seven Coniferous Tree Species to Inoculation with H. annosum and H. parviporum Conidial Suspensions in Controlled Conditions

Two healthy looking trees with no signs of root rot or other diseases were selected in forest stands of central and eastern Latvia for each of the following tree species: Siberian larch (Larix sibirica Ledeb.), Picea abies, Picea sitchensis, Pinus contorta, Weymouth pine (Pinus strobus L.), Pinus sylvestris and Pseudotsuga menziesii [32]. All selected trees were without visible decay at stump level. Moreover, as Heterobasidion mycelium can be found 30–60 cm in advance of the discoloration [37,38], all discs used in the experiment were cut at least 1 m upward the stem basis. The age of trees was between 23 and 44 years. Wood discs were prepared in an area distant from forests by cutting the basal portion of stems (up to 2 m height from the root collar) into slices of 2–3 cm thick. Wood discs, 10.7–16.5 cm in diameter, were kept at −5 °C until the day prior to the experiment when they were thawed at room temperature.
Conidial suspensions for the experiment were obtained by mixing conidia of three isolates, each of H. annosum (No. 93186, No. 98040, No. 03058, Finland) and H. parviporum (No. 98036, No. 03129, No. 05029, Finland). All isolates were cultured in Petri dishes on malt extract agar medium for 3 weeks at 20 °C. Conidial suspensions for each Heterobasidion species were prepared in 0.5 L of tap water by washing the conidia several times from three Petri dishes. The number of conidia in the suspension was calculated by counting conidia within 30 sight fields per Petri dish in Hagem agar medium in two repetitions under a microscope (magnification 100×) [39]. Conidial concentration in the suspensions was 42.16 × 103 conidia/mL of water for H. annosum and 45.83 × 103 conidia/mL of water for H. parviporum.
The experiment was performed on 26 August 2008. The surface of each wood disc was divided into four sectors. Sectors were numbered clockwise (No. 1–4), and sector No. 1 and sector No. 3 (opposite sectors) were treated with conidial suspensions of either H. annosum or H. parviporum (Figure 1) by using a sprayer. The other sectors were covered with a sheet of paper during treatment. Three wood discs for each tree species were treated with conidial suspensions of both fungal pathogens.
After treatments, each disc was placed individually in a loosely closed plastic bag and incubated for 7 days in the dark at room temperature. After incubation, discs were inspected for the presence of typical conidiophores of Heterobasidion spp. by using a dissecting microscope with 20–30 magnification, as previously described [24]. The area colonized by Heterobasidion spp. was marked. Afterwards, discs were scanned, and areas were measured using a planimeter (PLANIX 10S ‘Marble’, Tamaya, Japan). Borders between the sapwood and heartwood in each disc were visually determined by the same person.

2.2. Comparative Susceptibility of Wood Discs of Seven Coniferous Tree Species to Heterobasidion spp. Natural Airborne Infections and Rates of Infection at Increasing Distance from Spore Sources

2.2.1. Study Areas and Characterization of Heterobasidion annosum s.l. Disease Centres

Experiments were established in two sample plots: Kalsnava and Tireli. The Kalsnava plot was located in the eastern part of Latvia (56°41′9” N, 25°55′40” E). It represented a 76-year-old Norway spruce stand on drained peat soil (forest type Oxalidosa turf. mel.) with an admixture of Scots pine, silver birch (Betula pendula Roth) and black alder (Alnus glutinosa (L.) Gaertn.). The Tireli sample plot (56°50′35″ N, 23°47′51″ E) was located in a 30-year-old Norway spruce stand with an admixture of P. sylvestris on drained mineral soil (forest type Oxalidosa).
The Kalsnava sample plot was heavily infested by H. annosum s.l. At the center of the sample plot, in a radius of four meters, there was a windthrown Norway spruce tree with H. annosum s.l. fruiting bodies with a total area of hymenophores of 1431 cm2, two infected Norway spruce trees with fruiting bodies on the upper roots and a partly uplifted birch stump with H. annosum s.l. fruiting bodies under the roots. Some fruiting bodies were found at a distance of 20–40 m from the infection center. The total area of hymenophores of H. annosum s.l. fruiting bodies found in the Kalsnava sample plot was 2048 cm2. To identify the fungus at the species level, wood samples were taken with a sterilized increment borer or an axe from the windthrown Norway spruce, birch stump and from the roots of the infected Norway spruce.
In the Tireli sample plot, the H. annosum s.l. infection center was a gap of 8 m radius containing six Scots pine stumps. At the margin of the gap, there were five Scots pines with symptoms of H. annosum s.l. infection (thin crown). At the center of the gap, in a 3 m radius, four Scots pine stumps were located, two of them partly uplifted, with H. annosum s.l. fruiting bodies on the roots showing hymenophores with a total area of 485 cm2. Wood samples were collected from these two Scots pine stumps according to the method described above for the Kalsnava sample plot.
Isolations from wood samples were made according to Arhipova et al. [40]. Isolates were identified at the species level by assessing their ability to heterokaryotize the homokaryotic tester strains No. 05247 (H. annosum) and 05146 (H. parviporum) [41], kindly provided by Kari Korhonen. All isolates obtained from Tireli belonged to H. annosum, and all those obtained from Kalsnava belonged to H. parviporum.

2.2.2. Samplings to Determine the Susceptibility of Wood Discs to Heterobasidion annosum s.l. Natural Airborne Infections and the Rates of Spore Deposition at Increasing Distance from Spore Sources

In the Kalsnava sample plot, H. annosum s.l. spore deposition on wood discs was assessed along two transects in the four directions: north (N), south (S), east (E) and west (W) (Figure 2). The cross point of transects was established one meter from the largest Heterobasidion fruiting body group. The Tireli sample plot was located 20 m from a forest road, and therefore, spore deposition on wood discs was assessed along a single transect oriented south-east (SE) and north-west (NW) (Figure 2).
Four and two sampling campaigns were conducted at different time periods in Kalsnava and Tireli sample plots, respectively (Table 1). Ten wood discs prepared as described above were placed in each sampling period at each sampling point (two discs of P. sitchensis, two discs of P. menziesii, one disc of P. abies, one disc of P. sylvestris, two discs of P. contorta, one disc of P. strobus and one disc of L. sibirica) as summarized in Figure 2. Two discs of some species instead of one were used because of their smaller diameter. In total, 520 discs were exposed in the Kalsnava sample plot and 159 discs in the Tireli sample plot. At all sampling points, discs were placed on transparent plastic sheets during exposition to avoid any contamination originating from the ground. In all experiments, wood discs were exposed for approximately 17 h (4 p.m.–9 a.m.) (Table 1).
After exposure, each disc was placed individually in a plastic bag and brought to the laboratory. Discs were incubated for 7 days in loosely closed plastic bags at room temperature. Discs were inspected by using a dissecting microscope for the presence of H. annosum s.l. as described above.
Additionally, in order to explore the levels of spore deposition at increasing distance from spore sources in a way unbiased by the woody substrate, in the Kalsnava sample plot, a Petri dish filled with malt extract agar was placed directly under the largest H. annosum s.l. fruiting body so that the margin of the Petri dish gently touched its hymenophore. Additional Petri dishes were placed on the ground at 1 m distance from the largest H. annosum s.l. fruiting body group and in four directions (N, S, E, W) at a distance of 10 m and 30 m. Petri dishes were exposed during the daytime on 7 and 14 October 2008 for 1, 2, 4 and 8 min. Air temperature during exposure in these two days was 8 °C and 10 °C, respectively. The following day, spore counts were performed using light microscopy in 30 random sight fields in the Petri dish on Hagem agar medium.

2.3. Calculations and Statistics

In the experiment carried out under controlled conditions, the area colonized by either H. annosum or H. parviporum on the total surface of discs sprayed with conidial suspensions of either species (%) was determined. The sapwood area was calculated by subtraction of the heartwood area from the total area of the disc. Areas colonized by Heterobasidion spp. in sapwood and heartwood of wood discs (treated sectors) of different tree species were compared using non-parametric Mann–Whitney tests.
In the experiments carried out in the field, infection frequency expressed as the percentage of infected discs on the total number of discs exposed was compared between tree species in each sample plot using a chi-square test. The mean area occupied by H. annosum s.l. (percentage of the total area of the disc) in discs of each tree species, hereafter referred to as infection rate, was calculated for all discs in each sample plot (Kalsnava and Tireli). The correlation between the mean area occupied by Heterobasidion in different tree species and distances from the largest H. annosum s.l. fruiting body group was explored using Spearman’s rank-order correlation test.
The correlation between the mean proportion of area occupied by H. annosum s.l. on wood discs of different tree species after treating discs with conidial suspensions (data from H. annosum and H. parviporum pooled together) and by exposing discs in the field (data from Kalsnava and Tireli pooled together) was determined by using Spearman’s rank-order correlation test.
H. annosum s.l. basidiospores deposition in Petri dishes was calculated taking into account the number of spores, the area of sight field, the area of the Petri dish and the exposure time. Spore deposition was expressed per m2 in one hour (h). Data analyses were performed by using R 3.6.1 [42].

3. Results

3.1. Comparative Susceptibility of Wood Discs of Seven Coniferous Tree Species to H. annosum and H. parviporum Conidial Suspensions in Controlled Conditions

Heterobasidion annosum colonized a larger area than H. parviporum on wood discs of all the tested tree species except P. contorta, although differences were significant only for wood discs of P. abies (p < 0.05). The area occupied by H. parviporum was significantly larger in P. contorta compared to P. sitchensis and L. sibirica (p < 0.05) (Figure 3). The area occupied by H. parviporum in P. menziesii was significantly smaller compared to P. contorta, P. sylvestris, P. abies and P. strobus (p < 0.05).
The area occupied by H. annosum in P. sitchensis was significantly smaller compared to that in P. contorta (p < 0.05). The area occupied by H. annosum in P. menziesii was significantly smaller than that in P. contorta, P. sylvestris, P. abies and P. sitchensis (p < 0.05).
The overall areas colonized by either H. annosum or H. parviporum on wood discs of different tree species were correlated (r = 0.75, p = 0.052). In the discs of all the tree species and for both Heterobasidion species, the area colonized by the fungi in sapwood was much greater than that colonized in heartwood (Table 2).

3.2. Comparative Susceptibility of Wood Discs of Seven Coniferous Tree Species to H. annosum s.l. Natural Airborne Infections

At Kalsnava, more discs were infected in the first and second experiment compared to the third and fourth experiment: 97% and 98% compared to 77% and 84%, respectively. Most frequently, P. strobus, P. sylvestris and P. abies discs were infected: 100%, 96% and 89%, respectively. The proportion of infected L. sibirica, P. contorta, P. menziesii and P. sitchensis discs was comprised between 83% and 87% (Table 3).
At Tireli, the average infection frequency of wood discs was 88% and 75% in the first and second experiment, respectively. The wood discs of P. sylvestris were the most frequently infected (100%), whereas only 60% of wood discs of P. menziesii and 69% of those of L. sibirica were infected by H. annosum s.l. The frequency of infected P. abies, P. sitchensis, P. contorta and P. strobus wood discs was comprised between 82% and 88% (Table 3).
The area occupied by H. annosum s.l. on discs exposed in the Kalsnava sample plot was significantly greater (p < 0.05) than that on discs exposed in the Tireli sample plot for all tree species (Figure 4). In both Kalsnava and Tireli, the mean area occupied by H. annosum s.l. on wood discs was greater for P. contorta and P. sylvestris and lower for P. menziesii.
At Kalsnava, the area occupied by H. annosum s.l. in wood discs of P. sylvestris was significantly larger compared to that occupied in wood discs of P. abies, L. sibirica and P. menziesii (p < 0.05). The area occupied by H. annosum s.l. in wood discs of P. menziesii was significantly smaller compared to that in wood discs of P. strobus and P. contorta (p < 0.05). The area occupied by H. annosum s.l. in heartwood was small—the average for the analyzed tree species ranged from 0.01% to 0.55%, and there were no significant differences between tree species (p > 0.05).
At Tireli, the largest area occupied by H. annosum s.l. was in discs of P. sylvestris and P. contorta: 2.12% and 1.38% of the total surface of discs, respectively. The smallest occupied area was for P. menziesii—0.05%. The mean area occupied by H. annosum s.l. in discs of the other tree species ranged from 0.31% to 0.65%. At Tireli, no H. annosum s.l. infection was detected in the heartwood of any wood disc.
A positive and significant correlation was found between areas colonized by H. annosum s.l. on wood discs of different tree species in Kalsnava and Tireli sample plots (r = 0.90, p < 0.05). A positive and significant correlation was also found between the mean area occupied by H. annosum s.l. on discs treated with conidial suspensions in controlled conditions and on discs exposed in the forest plots of Kalsnava and Tireli (r = 0.79; p < 0.05).

3.3. Rates of Infection at Increasing Distance from Spore Sources in the Field

By analyzing the rates of infection of wood discs at different distances from the largest H. annosum s.l. fruiting body group at Kalsnava, a rapid decrease in the rate of infection of wood discs with distance was observed for most of the analyzed tree species and as an average (Figure 5). In the W direction, P. sylvestris and P. contorta showed higher rates of infection at a distance of 20 m compared to the other tree species. At 40 m distance in the S direction, a peak in rates of infection was observed for all tree species.
In Tireli, the highest infection rate in the first experiment was observed in the NW direction 5 m far from H. annosum s.l. fruiting bodies. In the second experiment, the highest infection rate was also observed in the NW direction at a distance of 1 m from H. annosum s.l. fruit bodies, and at a distance of 5 m. The infection rate decreased rapidly with distance from H. annosum s.l. fruiting bodies.
The levels of spore deposition under fruiting bodies of H. parviporum in Kalsnava determined by using Petri dishes was 87.17 × 106 spores per m2h−1 on 7 October and 12.85 × 106 spores per m2h−1 on 14 October (average 50.01 × 106 spores m2h−1). On 7 October, spore deposition attained more than one million spores per m2h−1 at a distance of 1 m from spore sources, and 82,250 and 61,688 spores m2h−1 at distances of 10 and 30 m from spore sources, respectively. On 14 October, spore deposition was more than 400,000 spores m2h−1 at a 1-m distance from spore sources and varied between 4113 and 41,125 spores m2h−1 at a distance of 10 m from the spore sources. At a distance of 30 m from spore sources, no spores were detected in any direction on 14 October.

4. Discussion

Our data shows variation in susceptibility of wood discs of different tree species to primary infection by H. annosum s.l., and, in this regard, results obtained by exposing discs to airborne infections in the forest are fully consistent with those of artificial inoculations in controlled conditions using conidial suspensions.
In comparative inoculation experiments on wood discs in controlled conditions using conidial suspensions, larger surfaces were colonized by H. annosum s.l. on wood discs of P. sylvestris, P. strobus and P. abies, and smaller in wood discs of P. menziesii. These findings support previous reports by Thomsen and Jacobsen [29], who observed higher growth rate of the fungus following artificial inoculation on wood discs of Scots pine and Norway spruce, followed by Douglas fir and hybrid larch. Nevertheless, in that study, the slowest growth rate was observed on Sitka spruce. Interestingly, on wood discs of Norway spruce, a significantly larger area was occupied by H. annosum compared to H. parviporum, despite many studies suggested that H. parviporum is better adapted to Norway spruce wood than H. annosum [43,44,45,46]. However, it should be noted that the development of Heterobasidion spp. on wood may vary depending on whether trees are alive or dead. In an experiment conducted in Latvia by inoculating Norway spruce billets with the same two Heterobasidion species [32], a slower growth rate was found for H. parviporum compared to H. annosum. In addition, a higher rate of isolation of H. annosum compared to H. parviporum was observed following primary infection on Norway spruce stumps in subalpine stands heavily infested by H. parviporum [47], supporting the hypothesis that H. annosum may be a better saprobe than H. parviporum, as previously documented on the wood blocks in laboratory conditions [48].
When exposing wood discs in the forest at Kalsnava and Tireli to H. annosum s.l. natural airborne infections, the fungus colonized the largest areas on wood discs of pine species, followed by P. sitchensis, P. abies and L. sibirica. Again, the smallest areas colonized by the fungus were found on wood discs of P. menziesii. Thus, our findings are in agreement with data obtained by Dimitri et al. [30] and Wang et al. [26], who reported higher susceptibility to H. annosum s.l. airborne infections of pine discs compared to Norway spruce discs. However, this is not consistent with the results of studies conducted in the Alps reporting higher infection frequencies in Norway spruce stumps compared to pine stumps [18]. More infected Norway spruce stumps compared to pine stumps have also been found in mixed spruce–pine stands in Latvia [19], as well as in small diameter stumps after pre-commercial thinning [49,50]. The above inconsistencies could be related to the substrate that was analyzed—discs vs. stumps. Discs are more prone to drying, and this may have accounted for the inconsistencies. In addition, the discs analyzed in this study had different diameters, and therefore, they could have been subjected to different degrees of drying.
In our study, the area occupied by H. annosum s.l. on wood discs of P. contorta was larger compared to that occupied by the fungus on wood discs of P. sitchensis, which is consistent with data provided by Redfern [28] using stumps as a substrate. At the same time, our results pointing to a lower susceptibility of wood discs of Douglas fir to primary infections by H. annosum s.l. corroborate previous observations by Morrison and Johnson [51], who found less infection of Douglas fir stumps compared to Sitka spruce stumps after precommercial thinning.
Rönnberg et al. [52] concluded that in pine stumps H. annosum s.l. spore infection was mainly found in sapwood, whereas Oliva et al. [53] indicated that on Norway spruce stumps, the fungus develops both in sapwood and heartwood. In our study, wood discs of all coniferous tree species analyzed showed very little heartwood infection. Referring to P. sylvestris and P. abies, our observations are in agreement with those of other studies showing that H. annosum s.l. spore infection mainly occurs in sapwood [52,54,55,56,57,58]. Conversely, other studies documented higher infection of heartwood compared to sapwood in Sitka spruce [59,60]. This might be due to the different methodology we used, particularly the storage of the discs at a temperature below 0 °C. Although this methodology (even using wood discs 6–9 cm in diameter) had already been used in other studies [21,25], it is possible that the conditions during storage could have modified the properties of heartwood in some tree species.
The results obtained by spraying wood discs with conidial suspensions in controlled conditions are in good agreement with those obtained by exposing wood discs to the natural airborne inoculum in the forests, as clearly supported by the significant correlations between the two sets of data. In both cases, these data suggest higher susceptibility to primary infections by H. annosum s.l. for P. contorta and other Pinus and Picea species, followed by L. sibirica, and lower susceptibility for P. menziesii.
The results obtained in this study, both through the comparative inoculation experiments of conidia on wood discs in controlled conditions and by exposing wood discs to H. annosum s.l. natural airborne infections in the two Norway spruce stands are in agreement with the results obtained by Zaluma et al. [32], who investigated the development of H. annosum s.l. mycelia in the wood of different tree species. In this latter study, a relevant H. annosum s.l. mycelium development deep in the wood was found with P. sylvestris, P. strobus and P. abies, an intermediate with P. contorta and P. sitchensis, and a limited development with L. sibirica and P. menziensii. It should be noted that the similarity of results between our study and the study by Zaluma et al. [32], who also used conidial suspensions of both H. annosum and H. parviporum, was more pronounced for the inoculation experiment with conidia of H. parviporum in controlled conditions and for discs exposed in the Kalsnava plot where, incidentally, all fruiting bodies sampled were identified as H. parviporum. Taken together, these findings suggest that it could be desirable to test the susceptibility of different Larix species to H. annosum s.l. in Latvian conditions. Larix sibirica is of particular interest because of a relatively limited development of H. annosum s.l. mycelia were observed in the wood of this tree species but, in contrast to P. menziesii, the development of Phlebiopsis gigantea—a well-known and effective antagonistic fungus against H. annosum s.l.—has been reported to occur in the wood of L. sibirica [32]. Other studies have also reported Larix spp. to be less susceptible to H. annosum s.l. compared to Norway spruce [17,18,61].
In our study, the highest rate of infection of most wood discs was identified at a distance of 1 m from the infection center, but at 5 and 10 m, the wood discs’ infection rates significantly decreased. This finding supports the results of investigations conducted in Fennoscandia [34,35], indicating that the maximum number of spores is released up to 10 m from the fruiting bodies. The exception to the above gradient in our study was the southern direction, where a significant increase in the infection rate was observed at a distance of 40 m. However, it should be noted that after additional surveys, initially undetected H. annosum s.l. fruiting bodies were found on rotten Norway spruce root fragments under the moss close to the points where discs were exposed. This confirms the importance of local spore sources in the prevalence of H. annosum s.l. infection in forest stands, as pointed out by several studies [20,23,35,36,62,63,64].
In this study, the spore load of H. annosum s.l. in a heavily infested Norway spruce stand was also analyzed using Petri dishes with agar medium. The number of spores observed in our study under the H. parviporum fruiting body was lower than that reported by Möykkynen et al. [21]. However, it should be noted that in this latter study conducted in Finland, the number of spores below the fruiting body was analyzed in June/August, at the peak of H. annosum s.l. sporulation in northern Europe [33], while in our study, samplings were conducted in October/November when sporulation is expected to be lower. In our study, the number of spores detected per m2 in different directions at a distance of 10–30 m from the largest group of fruiting bodies varied widely from 0 to 131600 spores. Other studies have also reported a relatively large variation in spores’ deposition levels in Norway spruce stands: 0–447 spores m2 h−1 [25] and 40–1500 spores m2 h−1 [30].
In conclusion, this study provides evidence that woods of different tree species differ in their susceptibility to primary infection by both H. annosum and H. parviporum. This study also supports the notion of a limited dispersal range of H. annosum s.l. basidiospores, pointing to the importance of local spore sources in the epidemiology of these pathogens.

Author Contributions

Conceptualization, T.G. and P.G.; methodology, T.G. and K.K.; validation, T.G.; formal analysis, G.L., K.K. and L.B.; investigation, K.K., D.K., N.B. and A.Z.; data curation, G.L., K.K. and L.B.; writing—original draft preparation, L.B.; writing—review and editing, P.G.; visualization, K.K.; supervision, T.G. and P.G.; project administration, N.B.; funding acquisition, N.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by European Regional Development Fund’s Research project No. 1.1.1.1/20/A/095 “Biological control of Heterobasidion root rot using Latvian fungal strains.”.

Data Availability Statement

Data is contained within the article and can be provided contacting corresponding author.

Acknowledgments

The authors acknowledge Kristīne Pāruma, Alīna Mihailova and Barbara Daugaviete for assistance in the field and laboratory work and Dainis Edgars Ruņģis for language revision. The authors are grateful to Kari Korhonen for providing Heterobasidiodion annosum and H. parviporum isolates used in this study and for providing useful comments on the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Garbelotto, M.; Gonthier, P. Biology, Epidemiology, and Control of Heterobasidion Species Worldwide. Annu. Rev. Phytopathol. 2013, 51, 39–59. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Korhonen, K.; Holdenrieder, O. Neue Erkenntnisse über den Wurzelschwamm (Heterobasidion annosum s.l.). Forst Holz 2005, 5, 206–211. (In German) [Google Scholar]
  3. Korhonen, K.; Bobko, I.; Hanso, S.; Piri, T.; Vasiliauskas, A. Intersterility groups of Heterobasidion annosum in some spruce and pine stands in Byelorussia, Lithuania and Estonia. Eur. J. For. Pathol. 1992, 22, 384–391. [Google Scholar] [CrossRef]
  4. Witzell, J.; Berglund, M.; Rönnberg, J. Does temperature regime govern the establishment of Heterobasidion annosum in Scandinavia? Int. J. Biometeorol. 2011, 55, 275–284. [Google Scholar] [CrossRef] [PubMed]
  5. Korhonen, K.; Capretti, P.; Karjalainen, R.; Stenlid, J. Distribution of Heterobasidion intersterility groups in Europe. In Heterobasidion annosum: Biology, Ecology, Impact and Control; Woodward, S., Stenlid, J., Karjalainen, R., Hüttermann, A., Eds.; CAB International: Wallingford, UK, 1998; pp. 93–104. [Google Scholar]
  6. Lygis, V.; Vasiliauskas, R.; Stenlid, J. Planting Betula pendula on pine sites infested by Heterobasidion annosum: Disease transfer, silvicultural evaluation, and community of wood-inhabiting fungi. Can. J. For. Res. 2004, 34, 120–130. [Google Scholar] [CrossRef]
  7. Asiegbu, F.O.; Adomas, A.; Stenlid, J. Conifer root and butt rot caused by Heterobasidion annosum (Fr.) Bref. s.l. Mol. Plant. Pathol. 2005, 6, 395–409. [Google Scholar] [CrossRef] [PubMed]
  8. Gonthier, P.; Warner, R.; Nicolotti, G.; Mazzaglia, A.; Garbelotto, M.M. Pathogen introduction as a collateral effect of military activity. Mycol. Res. 2004, 108, 468–470. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  9. Gonthier, P.; Nicolotti, G.; Linzer, R.; Guglielmo, F.; Garbelotto, M.M. Invasion of European pine stands by a North American forest pathogen and its hybridization with a native interfertile taxon. Mol. Ecol. 2007, 16, 1389–1400. [Google Scholar] [CrossRef] [PubMed]
  10. Gonthier, P.; Anselmi, N.; Capretti, P.; Bussotti, F.; Feducci, M.; Giordano, L.; Honorati, T.; Lione, G.; Luchi, N.; Michelozzi, M.; et al. An integrated approach to control the introduced forest pathogen Heterobasidion irregulare in Europe. Forestry 2014, 87, 471–481. [Google Scholar] [CrossRef] [Green Version]
  11. Gonthier, P.; Thor, M. Annosus root and butt rots. In Infectious Forest Diseases; Gonthier, P., Nicolotti, G., Eds.; CAB International: Wallingford, UK; New York, NY, USA, 2013; pp. 128–158. [Google Scholar]
  12. Greig, B.J.W. Species susceptibility to Fomes butt-rot. Q. J. For. 1979, 73, 21–25. [Google Scholar]
  13. Pratt, J.E.; Greig, B.J.W. Heterobasidion annosum: Development of butt rot following thinning in two young first rotation stands of Norway spruce. Forestry 1988, 61, 339–347. [Google Scholar] [CrossRef]
  14. Rönnberg, J.; Vollbrecht, G.; Thomsen, I.M. Incidence of butt rot in a tree species experiment in Northern Denmark. Scand. J. For. Res. 1999, 14, 234–239. [Google Scholar] [CrossRef]
  15. Greig, B.J.W.; Gibbs, J.N.; Pratt, J.E. Experiments on the susceptibility of conifers to Heterobasidion annosum in Great Britain. For. Pathol. 2001, 31, 219–228. [Google Scholar] [CrossRef]
  16. Lygis, V.; Vasiliauskaite, I.; Stenlid, J.; Vasaitis, R. Impact of forest fire on occurrence of Heterobasidion annosum s.s. root rot and other wood-inhabiting fungi in roots of Pinus mugo. Forestry 2010, 83, 83–92. [Google Scholar] [CrossRef] [Green Version]
  17. Gonthier, P.; Brun, F.; Lione, G.; Nicolotti, G. Modelling the incidence of Heterobasidion annosum butt rots and related economic losses in alpine mixed naturally regenerated forests of northern Italy. For. Pathol. 2012, 42, 57–68. [Google Scholar] [CrossRef]
  18. Gonthier, P. Frequency of stump infections by Heterobasidion annosum s.l. and benefits from urea treatments vary with tree species and season in European Alpine forests. For. Ecol. Manag. 2019, 434, 76–86. [Google Scholar] [CrossRef]
  19. Kenigsvalde, K.; Brauners, I.; Korhonen, K.; Zaļuma, A.; Mihailova, A.; Gaitnieks, T. Evaluation of the biological control agent Rotstop in controlling the infection of spruce and pine stumps by Heterobasidion in Latvia. Scand. J. For. Res. 2016, 31, 254–261. [Google Scholar] [CrossRef]
  20. Rishbeth, J. Dispersal of Fomes annosus Fr. and Peniophora gigantea (Fr.) Massee. Trans. Br. Mycol. Soc. 1959, 42, 243–260. [Google Scholar] [CrossRef]
  21. Möykkynen, T.; Von Weissenberg, K.; Pappinen, A. Estimation of dispersal gradients of S- and P-type basidiospores of Heterobasidion annosum. Eur. J. For. Pathol. 1997, 27, 291–300. [Google Scholar] [CrossRef]
  22. La Porta, N.; Ambrosi, P.; Grillo, R.; Korhonen, K. A study on the inoculum potential of Heterobasidion annosum in conifer stands of Alpine forests. In Proceedings of the 5th Congress of European Foundation for Plant Pathology: Biodiversity in Plant Pathology, Taormina, Italy, 18–22 September 2000; Catara, A., Albanese, G., Catara, V., La Rosa, R., Polizzi, G., Tessitori, M., Eds.; Societa Italiana di Patologia Vegetele: Pisa, Itay, 2001; pp. 289–294. [Google Scholar]
  23. Gonthier, P.; Garbelotto, M.M.; Varese, G.C.; Nicolotti, G. Relative abundance and potential dispersal range of intersterility groups of Heterobasidion annosum in pure and mixed forests. Can. J. Bot. 2001, 79, 1057–1065. [Google Scholar] [CrossRef]
  24. Gonthier, P.; Garbelotto, M.M.; Nicolotti, G. Seasonal patterns of spore deposition of Heterobasidion species in four forests of the western Alps. Phytopathology 2005, 95, 759–767. [Google Scholar] [CrossRef] [Green Version]
  25. Möykkynen, T.; Kontiokari, J. Spore deposition of Heterobasidion annosum coll. in Picea abies stands of North Karelia, eastern Finland. For. Pathol. 2001, 31, 107–114. [Google Scholar] [CrossRef]
  26. Wang, L.Y.; Pålsson, H.; Ek, E.; Rönnberg, J. The effect of Phlebiopsis gigantea and urea stump treatment against spore infection of Heterobasidion spp. on hybrid larch (Larix × eurolepis) in southern Sweden. For. Pathol. 2012, 42, 420–428. [Google Scholar] [CrossRef]
  27. Pellicciaro, M.; Lione, G.; Giordano, L.; Gonthier, P. Biocontrol potential of Pseudomonas protegens against Heterobasidion species attacking conifers in Europe. Biol. Control. 2021, 157, 104583. [Google Scholar] [CrossRef]
  28. Redfern, D.B. Infection of Picea sitchensis and Pinus contorta stumps by basidiospores of Heterobasidion annosum. Eur. J. For. Pathol. 1982, 12, 11–25. [Google Scholar] [CrossRef]
  29. Thomsen, I.M.; Jacobsen, J.B. Testing of Rotstop on Sitka spruce, Douglas-fir and larch. In Root and Butt Rots of Forest Trees, Proceedings of the 10th International Conference on Root and Butt Rots: IUFRO WP 7.02.01, Québec City, QC, Canada, 16–22 September 2001; Laflamme, G., Bérubé, J.A., Bussières, G., Eds.; Canadian Forest Service: Sainte-Foy, QC, Canada, 2003; pp. 216–220. [Google Scholar]
  30. Dimitri, L.; Zycha, H.; Kliefoth, R. Untersuchungen über die Bedeutung der Stubbeninfektion durch Fomes annosus für die Ausbreitung der Rotfäule der Fichte. Forstwiss. Cent. 1971, 90, 104–117. (In German) [Google Scholar] [CrossRef]
  31. Jansons, J. Statistical Inventory of Resources of Forests of Latvia: Results of Cycle IV. Available online: http://www.silava.lv/petijumi/nacionlais-mea-monitorings.aspx (accessed on 25 March 2021). (In Latvian).
  32. Zaluma, A.; Bruna, L.; Klavina, D.; Burnevica, N.; Kenigsvalde, K.; Lazdins, A.; Gaitnieks, T. Growth of Phlebiopsis gigantea in wood of seven conifer species. For. Pathol. 2019, 49, e12555. [Google Scholar] [CrossRef]
  33. Brandtberg, P.-O.; Johansson, M.; Seeger, P. Effects of season and urea treatment on infection of stumps of Picea abies by Heterobasidion annosum in stands on former arable land. Scand. J. For. Res. 1996, 11, 261–268. [Google Scholar] [CrossRef]
  34. Kallio, T. Aerial distribution of the root-rot fungus Fomes annosus (Fr.) Cooke in Finland. Acta For. Fenn. 1970, 107, 7541. [Google Scholar] [CrossRef] [Green Version]
  35. Stenlid, J. Regional differentiation in Heterobasidion annosum. In Proceedings of the 8th international Conference on Root and Butt Rots, Wik, Sweden and Haikko, Finland, 9–16 August 1993; Johansson, M., Stenlid, J., Eds.; Swedish University of Agricultural Sciences: Uppsala, Sweden, 1994; pp. 243–248. [Google Scholar]
  36. Gonthier, P.; Lione, G.; Giordano, L.; Garbelotto, M. The American forest pathogen Heterobasidion irregulare colonizes unexpected habitats after its introduction in Italy. Ecol. Appl. 2012, 22, 2135–2143. [Google Scholar] [CrossRef] [Green Version]
  37. Bendz-Hellgren, M.; Brandtberg, P.O.; Johansson, M.; Swedjemark, G.; Stenlid, J. Growth rate of Heterobasidion annosum in Picea abies established on forest land and arable land. Scand. J. For. Res. 1999, 14, 402–407. [Google Scholar] [CrossRef]
  38. Piri, T. Early development of root rot in young Norway spruce planted on sites infected by Heterobasidion in southern Finland. Can. J. For. Res. 2003, 33, 604–611. [Google Scholar] [CrossRef]
  39. Bruna, L.; Klavina, D.; Zaluma, A.; Kenigsvalde, K.; Burneviča, N.; Nikolajeva, V.; Gaitnieks, T.; Piri, T. Efficacy of Phlebiopsis gigantea against Heterobasidion conidiospore and basidiospore infection in spruce wood. iForest Biogeosci. For. 2020, 13, 369–375. [Google Scholar] [CrossRef]
  40. Arhipova, N.; Gaitnieks, T.; Donis, J.; Stenlid, J.; Vasaitis, R. Butt rot incidence, causal fungi, and related yield loss in Picea abies stands of Latvia. Can. J. For. Res. 2011, 41, 2337–2345. [Google Scholar] [CrossRef]
  41. Korhonen, K. Intersterility Groups of Heterobasidion Annosum; Metsäntutkimuslaitoksen Julkaisuja; Valtioneuvoston Kirjapaino: Helsinki, Finland, 1978; Volume 94, pp. 1–25. [Google Scholar]
  42. R CoreTeam. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2019; Available online: https://www.R-project.org/ (accessed on 3 September 2020).
  43. Vasiliauskas, R.; Stenlid, J. Spread of S and P group isolates of Heterobasidion annosum within and among Picea abies trees in central Lithuania. Can. J. For. Res. 1998, 28, 961–966. [Google Scholar] [CrossRef]
  44. Korhonen, K. Simulated stump treatment experiments for monitoring the efficacy of Phlebiopsis gigantea against Heterobasidion annosum. In Root and Butt Rots of Forest Trees, Proceedings of the 10th International Conference on Root and Butt Rots: IUFRO WP 7.02.01, Québec City, QC, Canada, 16–22 September 2001; Laflamme, G., Bérubé, J.A., Bussières, G., Eds.; Canadian Forest Service: Sainte-Foy, QC, Canada, 2003; pp. 206–210. [Google Scholar]
  45. Oliva, J.; Bendz-Hellgren, M.; Stenlid, J. Spread of Heterobasidion annosum s.s. and Heterobasidion parviporum in Picea abies 15 years after stump inoculation. FEMS Microbiol. Ecol. 2011, 75, 414–429. [Google Scholar] [CrossRef]
  46. Zaluma, A.; Gaitnieks, T.; Arhipova, N.; Vasaitis, R. Growth rates of Heterobasidion annosum s.s. and H. parviporum in functional sapwood of Pinus sylvestris and Picea abies. For. Pathol. 2015, 45, 437–439. [Google Scholar] [CrossRef]
  47. Gonthier, P.; Garbelotto, M.M.; Nicolotti, G. Swiss stone pine trees and spruce stumps represent an important habitat for Heterobasidion spp. in subalpine forests. For. Pathol. 2003, 33, 191–203. [Google Scholar] [CrossRef] [Green Version]
  48. Daniel, G.; Asiegbu, F.O.; Johansson, M. The saprotrophic wood-degrading abilities of Heterobasidium annosum intersterility groups P and S. Mycol. Res. 1998, 102, 991–997. [Google Scholar] [CrossRef]
  49. Gaitnieks, T.; Brauners, I.; Kenigsvalde, K.; Zaļuma, A.; Brūna, L.; Jansons, J.; Burņeviča, N.; Lazdiņš, A.; Vasaitis, R. Infection of pre-commercially cut stumps of Picea abies and Pinus sylvestris by Heterobasidion spp.—A comparative study. Silva. Fenn. 2018, 52, 1–7. [Google Scholar] [CrossRef]
  50. Gaitnieks, T.; Zaļuma, A.; Kenigsvalde, K.; Brūna, L.; Kļaviņa, D.; Burņeviča, N.; Stenlid, J.; Jankovský, L.; Vasaitis, R. Natural infection and colonization of pre-commercially cut stumps of Picea abies and Pinus sylvestris by Heterobasidion rot and its biocontrol fungus Phlebiopsis gigantea. Biol. Control. 2020, 143, 104208. [Google Scholar] [CrossRef]
  51. Morrison, D.J.; Johnson, A.L.S. Incidence of Heterobasidion annosum in precommercial thinning stumps in coastal British Columbia. Eur. J. For. Pathol. 1999, 29, 1–16. [Google Scholar] [CrossRef]
  52. Rönnberg, J.; Petrylaite, E.; Nilsson, G.; Pratt, J. Two studies to assess the risk to Pinus sylvestris from Heterobasidion spp. in southern Sweden. Scand. J. For. Res. 2006, 21, 405–413. [Google Scholar] [CrossRef]
  53. Oliva, J.; Bernat, M.; Stenlid, J. Heartwood stump colonisation by Heterobasidion parviporum and H. annosum s.s. in Norway spruce (Picea abies) stands. For. Ecol. Manag. 2013, 295, 1–10. [Google Scholar] [CrossRef]
  54. Swedjemark, G.; Stenlid, J. Population Dynamics of the Root Rot Fungus Heterobasidion annosum Following Thinning of Picea abies. Oikos 1993, 66, 247. [Google Scholar] [CrossRef]
  55. Nicolotti, G.; Gonthier, P.; Varese, G.C. Effectiveness of some biocontrol and chemical treatments against Heterobasidion annosum on Norway spruce stumps. Eur. J. For. Pathol. 1999, 29, 339–346. [Google Scholar] [CrossRef]
  56. Johansson, S.M.; Pratt, J.E.; Asiegbu, F.O. Treatment of Norway spruce and Scots pine stumps with urea against the root and butt rot fungus Heterobasidion annosum—Possible modes of action. For. Ecol. Manag. 2002, 157, 87–100. [Google Scholar] [CrossRef]
  57. Berglund, M.; Rönnberg, J. Effectiveness of treatment of Norway spruce stumps with Phlebiopsis gigantea at different rates of coverage for the control of Heterobasidion. For. Pathol. 2004, 34, 233–243. [Google Scholar] [CrossRef]
  58. Rönnberg, J.; Sidorov, E.; Petrylaite, E. Efficacy of different concentrations of Rotstop® and Rotstop®S and imperfect coverage of Rotstop®S against Heterobasidion spp. spore infections on Norway spruce stumps. For. Pathol. 2006, 36, 422–433. [Google Scholar] [CrossRef]
  59. Redfern, D.B. The effect of wood moisture on infection of Sitka spruce stumps by basidiospores of Heterobasidion annosum. Eur. J. For. Pathol. 1993, 23, 218–235. [Google Scholar] [CrossRef]
  60. Redfern, D.B.; Pratt, J.E.; Gregory, S.C.; MacAskill, G.A. Natural infection of Sitka spruce thinning stumps in Britain by spores of Heterobasidion annosum and long-term survival of the fungus. Forestry 2001, 74, 53–72. [Google Scholar] [CrossRef] [Green Version]
  61. Gonthier, P. Controlling root and butt rot diseases in Alpine European forests. In Management of Fungal Plant Pathogens; Arya, A., Pereló, A.E., Eds.; CABI Internationl: Wallingford, UK, 2010; pp. 345–361. ISBN 9781845936037. [Google Scholar]
  62. Rishbeth, J. Observations on the Biology of Fomes annosus, with Particular Reference to East Anglian Pine Plantations: II. Spore production, stump infection, and a saprophytic activity in stumps. Ann. Bot. 1951, 15, 1–22. [Google Scholar] [CrossRef]
  63. Yde-Anersen, A. Seasonal Incidence of Stump Infection in Norway Spruce by Air-Borne Fomes annosus Spores. For. Sci. 1962, 8, 98–103. [Google Scholar] [CrossRef]
  64. Redfern, D.B.; Pratt, J.E.; Whiteman, A. Stump treatment against Heterobasidion annosum: A re-appraisal. In Proceedings of the 8th International Conference on Root and Butt Rots, Wik, Sweden and Haikko, Finland, 9–16 August 1993; Johansson, M., Stenlid, J., Eds.; Swedish University of Agricultural Sciences: Uppsala, Sweden, 1994; pp. 656–661. [Google Scholar]
Forests 12 00854 g001 550
Figure 1. Spraying scheme of wood discs. Abbreviations: H.a.—area treated with Heterobasidion annosum conidial suspension; H.p.—area treated with H. parviporum conidial suspension.
Figure 1. Spraying scheme of wood discs. Abbreviations: H.a.—area treated with Heterobasidion annosum conidial suspension; H.p.—area treated with H. parviporum conidial suspension.
Forests 12 00854 g001
Forests 12 00854 g002 550
Figure 2. Location of sampling points and groups of Heterobasidion annosum s.l. fruiting bodies: (a) the Kalsnava sample plot and (b) the Tireli sample plot). Relative area of H. annosum s.l. fruiting body hymenophores; dashed line with arrow shows the cross point of transects located 1 m from the largest group of H. annosum s.l. fruiting bodies.
Figure 2. Location of sampling points and groups of Heterobasidion annosum s.l. fruiting bodies: (a) the Kalsnava sample plot and (b) the Tireli sample plot). Relative area of H. annosum s.l. fruiting body hymenophores; dashed line with arrow shows the cross point of transects located 1 m from the largest group of H. annosum s.l. fruiting bodies.
Forests 12 00854 g002
Forests 12 00854 g003 550
Figure 3. The mean area occupied by Heterobasidion annosum and H. parviporum on wood discs of seven coniferous tree species inoculated with conidial suspensions.
Figure 3. The mean area occupied by Heterobasidion annosum and H. parviporum on wood discs of seven coniferous tree species inoculated with conidial suspensions.
Forests 12 00854 g003
Forests 12 00854 g004 550
Figure 4. The mean area occupied by Heterobasidion annosum s.l. on wood discs of different tree species exposed in the forest plots of Kalsnava and Tireli.
Figure 4. The mean area occupied by Heterobasidion annosum s.l. on wood discs of different tree species exposed in the forest plots of Kalsnava and Tireli.
Forests 12 00854 g004
Forests 12 00854 g005 550
Figure 5. The rates of infection of wood discs of seven coniferous tree species by Heterobasidion annosum s.l. in the Kalsnava sample plot at increasing distances from spore sources. Disc exposition in different directions—(a) east, (b) north, (c) west and (d) south; only in figure (a) the area occupied by Heterobasidion annosum s.l. at a distance “1 m” from the largest group of fruiting bodies is shown; the same numbers refer to other directions.
Figure 5. The rates of infection of wood discs of seven coniferous tree species by Heterobasidion annosum s.l. in the Kalsnava sample plot at increasing distances from spore sources. Disc exposition in different directions—(a) east, (b) north, (c) west and (d) south; only in figure (a) the area occupied by Heterobasidion annosum s.l. at a distance “1 m” from the largest group of fruiting bodies is shown; the same numbers refer to other directions.
Forests 12 00854 g005
Table
Table 1. Main features and experimental conditions of sampling campaigns of airborne Heterobasidion annosum s.l. spores in Kalsnava and Tireli.
Table 1. Main features and experimental conditions of sampling campaigns of airborne Heterobasidion annosum s.l. spores in Kalsnava and Tireli.
Sample PlotDate of Experiment in 2008Analyzed DirectionsDistance from the Group of Fruit Bodies, mAir Temperature, °CAir Humidity, %Speed (m/s) and Direction of Wind
Kalsnava15.07–16.07N, S, E, W1 *, 5, 10, 20, 30, 40, 5016801–3, SW
03.08–04.08N, S, E, W1, 10, 3018801–4, SW, W
11.08–12.08N, S, E, W1, 10, 3017891–3, S, SW
21.08–22.08N, S, E, W1, 20, 4015893–4, SW
Tireli30.08–31.08NW1, 5, 10, 301286, heavy rain1–4, NW
SE10, 20, 40
11.09–12.09NW1, 5, 10, 308723–4, NE
SE10, 20, 40
*: the transect cross point at the distance of 1 m from the largest H. annosum s.l. fruiting body group.
Table
Table 2. The percentage of the area occupied by Heterobasidion annosum and H. parviporum in the sapwood and heartwood of the discs of seven tree species.
Table 2. The percentage of the area occupied by Heterobasidion annosum and H. parviporum in the sapwood and heartwood of the discs of seven tree species.
Mean Area (%) Occupied by Heterobasidion spp.
Larix sibiricaPicea abiesPicea sitchensisPinus contortaPinus strobusPinus sylvestrisPseudotsuga menziesii
H. parviporumSapwood24.943.425.848.471.567.811.0
Heartwood0.12.14.70.00.20.00.1
H. annosumSapwood40.871.440.644.468.080.618.0
Heartwood0.56.33.00.51.80.010.1
Table
Table 3. The Heterobasidion annosum s.l. infection frequency (%) of wood discs of different tree species in the Kalsnava and Tireli study sites.
Table 3. The Heterobasidion annosum s.l. infection frequency (%) of wood discs of different tree species in the Kalsnava and Tireli study sites.
Tree SpeciesKalsnavaTireli
1 *234Average12Average
Larix sibirica96100676783885069
Picea abies100100678989888888
Picea sitchensis981007278871006985
Pinus contorta92100787286946982
Pinus strobus1001001001001007510088
Pinus sylvestris961008910096100100100
Pseudotsuga menziesii10089678385695060
Average9798778489887582
*: Experiment number 1 to 4.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Brūna, L.; Lione, G.; Kenigsvalde, K.; Burņeviča, N.; Zaļuma, A.; Kļaviņa, D.; Gaitnieks, T.; Gonthier, P. Inferences on the Susceptibility of Wood of Different Tree Species to Heterobasidion annosum Sensu Lato Primary Infections and on the Range of Pathogen Spores Dispersal. Forests 2021, 12, 854. https://doi.org/10.3390/f12070854

AMA Style

Brūna L, Lione G, Kenigsvalde K, Burņeviča N, Zaļuma A, Kļaviņa D, Gaitnieks T, Gonthier P. Inferences on the Susceptibility of Wood of Different Tree Species to Heterobasidion annosum Sensu Lato Primary Infections and on the Range of Pathogen Spores Dispersal. Forests. 2021; 12(7):854. https://doi.org/10.3390/f12070854

Chicago/Turabian Style

Brūna, Lauma, Guglielmo Lione, Kristīne Kenigsvalde, Natālija Burņeviča, Astra Zaļuma, Dārta Kļaviņa, Tālis Gaitnieks, and Paolo Gonthier. 2021. "Inferences on the Susceptibility of Wood of Different Tree Species to Heterobasidion annosum Sensu Lato Primary Infections and on the Range of Pathogen Spores Dispersal" Forests 12, no. 7: 854. https://doi.org/10.3390/f12070854

APA Style

Brūna, L., Lione, G., Kenigsvalde, K., Burņeviča, N., Zaļuma, A., Kļaviņa, D., Gaitnieks, T., & Gonthier, P. (2021). Inferences on the Susceptibility of Wood of Different Tree Species to Heterobasidion annosum Sensu Lato Primary Infections and on the Range of Pathogen Spores Dispersal. Forests, 12(7), 854. https://doi.org/10.3390/f12070854

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop