Fungal succession in sapwood of Norway spruce infested by the bark beetle Ips typographus

Fungal invasion of Norway spruce sapwood was investigated during a period of 130 weeks fol-lowing attack by the spruce bark beetle Ips typographus. Heavy beetle attack tended to overwhelm the trees quickly and no secondary resinosis was produced. Nonetheless, fungal penetration in the sapwood was initiated only slowly, although it accelerated during the fourth week after attack. Typically the leading edge of fungal penetration was a few millimeters in advance of the visible blue-stain during the sapwood colonization. Fungi invaded the sapwood in a successional pattern with the most pathogenic species Ophiostoma polonicum first, followed by other beetle-transmitted Ophiostoma and Graphium species. The later succession was probably influenced by sapwood moisture. Strong decaying white-rotters invaded near the base of the trees, where sapwood moisture remained favourable, while cf. Trichoderma viride dominated in the drier parts or the trees.     

Fungi isolated from Picea abies infested by the bark beetle Ips typographus in the Białowieża forest in north‐eastern Poland

The assemblage of fungi occurring in the sapwood of Norway spruce (Picea abies) and in bark beetle galleries following attack by the Eurasian spruce bark beetle Ips typographus was investigated in the Bia?owie?a forest in north‐eastern Poland. Fungi were isolated from blue‐stained sapwood of beetle‐infested spruce trees in June 2002, and a few isolates were also obtained from ascospores and conidia taken from perithecia and asexual structures occurring in the gallery systems of the insects. The mycobiota of I. typographus in the Bia?owie?a forest was dominated by ophiostomatoid fungi, which were represented by seven species. Four species, including Ceratocystis polonica, Grosmannia penicillata, Ophiostoma ainoae and Ophiostoma bicolor were isolated at high frequencies, whereas three other taxa, Ceratocystiopsis minuta, Ceratocystiopsis alba and a Pesotum sp. were rare. The anamorphic fungus Graphium fimbriisporum and yeasts also occurred occasionally. In addition, the basidiomycete Gloeocystidium ipidophilum was relatively common. The pathogenic blue‐stain fungus C. polonica was the dominant fungal associate of I. typographus in the Bia?owie?a forest, which is consistent with a previous study at this area in the 1930s. Ceratocystis polonica was the most frequently isolated species at the leading edge of fungal colonization in the sapwood and had on an average penetrated deeper into the wood than other fungal associates. This suggests that it acts as a primary invader into the sapwood after attack by I. typographus in the Bia?owie?a forest, followed by O. bicolor, O. ainoae, G. ipidophilum and G. penicillata. Thus far, the Bia?owie?a forest is one of the few areas in Europe, where C. polonica has been reported as a dominate fungal associate of I. typographus.     

Fungi associated with the spruce bark beetle Ips typographus in an endemic area in Norway

To investigate the fungal flora associated with the spruce bark beetle Ips typographus in an endemic area, beetles were collected during the flight period in six locations in Tr?ndelag, Norway. The beetles were inoculated into fresh Norway spruce logs, and the frequency of different species was monitored by fungal isolation from bark and wood. The most common species were Ophiostoma bicolor, O. penicillatum, O. polonicum and a previously undescribed Graphium species, the same species which were the most important associates of I. Typographus in an epidemic area in southeastern Norway. The frequency of the primary invader, O. polonicum, was, however, lower in Tr?ndelag, which may indicate that this species is less frequent in endemic areas than in epidemic areas.     

Attacks by Ips typographus and Pityogenes chalcographus on Windthrown Spruces (Picea abies) During the Two Years Following a Storm Felling

Attacks by Ips typographus and Pityogenes chalcographus during the first 2 yrs after a storm were studied on 1848 windthrown spruces (Picea abies) in southern Sweden. In the first and second summer, 29% and 24%, respectively, of the spruces were attacked by I. typographus, while 21% and 44%, respectively, were attacked by P. chalcographus. High stumps were attacked less frequently than tops, broken trees and windfelled trees with root contact. In both years, trunks in gaps were preferred over those in stands. The proportion of windthrown trees attacked by I. typographus increased with stem diameter, whereas the opposite was true for P. chalcographus. Positive interspecific associations between the species were found on the lower, middle and upper third parts of the trees in the first summer and on the lower part in the second summer. The results are discussed with regard to forest protection and nature conservation.     

Variation in sapwood thickness of Picea abies in Estonia depending on the tree age

Variation of sapwood thickness in terms of a linear measurement and a growth ring count with reference to the age was studied in dominant and suppressed Norway spruce trees. In the trees of both dominance classes the sapwood thickness increased in absolute terms, while its relative portion decreased with the age of the trees growing. Great differences were found in sapwood thickness between dominant and suppressed trees in linear measurements but not in the number of sapwood rings or the rate of the heartwood formation. The number of sapwood growth rings reached 40 in old trees. The index of vigour differed considerably in dominant and suppressed trees.     

Effect of phenolic compounds on the in vitro growth of two fungi associated with Ips typographus

The susceptibility of Ophiostoma piceaperdum (n = 17) and O. bicolor isolates (n = 7) to catechin and resveratrol has been investigated with growth bioassays on malt‐agar medium. While catechin (10^?3 m ) did not have any significant influence, resveratrol (10^?3 m ) inhibited the growth of the two species, particularly the growth of O. piceaperdum isolates. We did not observe any synergistic inhibitory effect between the two phenolic compounds. Significant differences either in fungal growth on malt agar medium or susceptibility to resveratrol occurred among isolates for both species. Our results corroborate previous observations of high genetic and virulence variability among isolates of ophiostomatoid fungi and indicate that further studies should take into account the intraspecific variability of the fungal species of this group.     

Testing the unifying theory of ozone sensitivity with mature trees of Fagus sylvatica and Picea abies

The broad range in plant responses to chronic O(3) exposure compels a search for integrative, underlying principles. One such approach is the unifying theory proposed by Reich (1987), which combines the O(3) response of contrasting physiognomic classes of plants on the basis of their intrinsic leaf diffusive conductance and, hence, capacity for O(3) uptake. Physiognomic classes differ in the proportional decline in photosynthesis and growth when compared on the basis of cumulative O(3) exposure per unit time, but converge when compared on the basis of O(3) uptake per unit time or cumulative O(3) uptake over the entire lifetime of the leaf. The theory is based on observations on a large number of contrasting plant species, relying primarily on studies of juvenile trees subjected to short-term O(3) exposure. To test the applicability of the unifying theory to mature trees, broadleaf deciduous European beech (Fagus sylvatica L.) and the evergreen conifer Norway spruce (Picea abies (L.) Karst.) in a mature mixed stand were exposed to either ambient air (control) or air with twice the ambient O(3) concentration delivered into the canopy by means of a free-air fumigation system. We accounted for differences in growing season length, leaf longevity and O(3)-related effects on leaf diffusive conductance in determining total O(3) uptake over the lifetime of the leaf. On this basis, Norway spruce needles required 5 years to take up as much O(3) as did beech leaves in one growing season. The core of the unifying theory on O(3) sensitivity was substantiated in relation to O(3) exposure and uptake. However, contrary to the unifying theory, which was formulated on the basis of results with juvenile trees, the O(3) response of mature trees in a natural stand was more complex. The increased complexity was attributed to additional environmental stressors, stress compensation at the whole-tree level, and differential O(3) sensitivities of leaves according to age class and position within the canopy. Contrary to the theory, photosynthesis was no less sensitive to O(3) in Norway spruce than that of beech, and was reduced in the twice-ambient O(3) regime in the first year of exposure.     

Effect of topography and geology on the site index of Picea abies in the West Carpathian,Poland

Abstract

The effects of topographic features and the soil parent rock on the site index of Norway spruce [Picea abies (L.) Karst.] were examined. Field data were collected on 347 plots located in the Polish West Carpathian. On these plots, the diameter at breast height and the height of trees were measured and the age of trees was determined. On 64 plots one dominant or codominant tree was felled for stem analysis. In addition, topographic features of each site were measured, including elevation above sea level, aspect and slope. Stem analysis data were used in the development of a local site index system, which was used for calculating the site index for particular plots. In order to interpret site index as functions of elevation, aspect, slope, size of a mountain massif and soil parent rock, the multiple regression model was used, which explained 79.0% of the variation in Norway spruce site index. Elevation above sea level was the major factor responsible for variation in site index, and was negatively correlated (R ² _adj=0.610) with site index. Site index also depended on the soil parent rock. The stands growing on the tertiary Magura sandstones had considerably higher site indices than those located on the geological substratum composed of Istebna and Godula sandstones formed during the Cretaceous period. The site index of Norway spruce is also determined by the aspect, slope and height of mountain massif.     

Changes in soluble-phenol content of Norway-spruce (Picea abies) phloem in response to wounding and inoculation with Ophiostoma polonicum

The aim of this study was to investigate the temporal changes in Norway-spruce (Picea abies) phloem phenolics during wound-induced response. Two Norway spruces were inoculated with Ophiostoma polonicum and sterile agar; unwounded phloem was simultaneously tested as control. Both unwounded and inoculated phloem were then sampled 6, 11, 21, 30, and 60 days later. Monophenols were analysed by HPLC, and the tanning capacity of the phloem extracts was estimated from their ability to precipitate proteins. The response to inoculation was characterized by radical changes in the phloem phenolic composition. Initially, an increase in (+)-catechin concentration was observed, concomitant with a slow decrease in both glycoside concentrations and tanning capacity. After day 6, this decrease was accelerated in the event of fungus inoculation. The appearance of aglycones did not take place during the decrease in glycosides, but was delayed. The phenolic response of Norway-spruce phloem to inoculation is modulated by the presence of the fungus and is focused on the formation of insoluble compounds.     

Retention of wind-felled trees and the risk of consequential tree mortality by the European spruce bark beetle Ips typographus in Finland

Abstract

Autumn storms felled about 7 million m³ of forest in southern Finland in 2001. Windthrow area and timber characteristics, as well as numbers of standing spruce trees attacked and killed by Ips typographus, were recorded in 61 Norway spruce [Picea abies (L.) Karst.]-dominated windthrow areas. Generalized linear models were used to identify significant variables predicting the risk for consequential tree mortality by I. typographus. None of the windthrow areas with fewer than 20 wind-felled spruce trees (WFS) (n=28) and only half of the areas with 20 or more WFS (n=33) harboured trees killed by I. typographus during the years 2003–2005. The quantity and diameter of WFS and the basal area of recently dead standing spruce trees correlated positively with the risk of tree deaths. This study indicates that in Finland, at endemic I. typographus population levels, it is safe to leave fewer than 20 WFS in managed forests. Retention of even larger quantities of trees does not seem to evoke significant numbers of consequential tree deaths by I. typographus in managed forests. However, in stands where the natural mortality of spruce trees is high, the risks of consequential tree deaths after wind disturbance will also be higher.     

Organic and inorganic sulfur transport in the xylem sap and the sulfur budget of Picea abies trees

Temporal changes in inorganic and organic sulfur compounds (sulfate, glutathione, cysteine, methionine) were analyzed in xylem sap of 40-year-old Norway spruce (Picea abies (L.) Karst.) trees growing on acidic soils at a healthy and a declining stand in the Fichtelgebirge (North Bavaria, Germany). Studies were carried out (1) to quantify glutathione (GSH) transport in the xylem of spruce, (2) to study the significance of reduced sulfur versus sulfate (SO(4) (2-)) transport in the xylem, and (3) to compare total sulfur (S) transport in the xylem with the amount of foliar uptake of SO(2) in an air-polluted environment. Glutathione was the main reduced S compound in the xylem ranging in concentration from 0.5 to 5 &mgr;mol l(-1). Concentrations of inorganic SO(4) (2-) in the xylem sap were up to 50 times higher than those of GSH ranging from 60 to 230 &mgr;mol l(-1). During the growing season, concentrations of all S compounds in the xylem were highest in May (up to 246 &mgr;mol l(-1)) and decreased during summer and fall (up to 21 &mgr;mol l(-1)). On average, SO(4) (2-) concentrations in xylem sap were 30% higher at the declining site compared with the healthy site. Diurnal changes in organic S compounds were significant for GSH and cysteine with high concentrations during the night and low concentrations during the day. Diurnal changes in inorganic concentrations were not significant. Xylem sap concentrations of SO(4) (2-) and cysteine were twice as high and GSH concentrations were tenfold higher in surface roots than in branches. At both sites, transport of organic S was low (up to 3% of total S) compared to transport of SO(4) (2-). Annual transport of total S in the xylem (SO(4) (2-) was the main component) ranged from 60 to 197 mmol tree(-1) year(-1) at the healthy site and from 123 to 239 mmol tree(-1) year(-1) at the declining site. Although gaseous uptake of SO(2) was estimated to be similar at both sites (38 mmol tree(-1) year(-1); Horn et al. 1989), the ratio between annual gaseous uptake of SO(2) and transport of S in the xylem was 1:4 and 1:5 at the healthy and declining sites, respectively.     

Growth rates of Heterobasidion annosum s.s. and H. parviporum in functional sapwood of Pinus sylvestris and Picea abies

Growth rates of H. annosum s.s. and H. parviporum were investigated in the functional sapwood of young Pinus sylvestris and Picea abies plants as an indicator of the relative susceptibilities of the hosts to these pathogens. The stems of 520 five‐year‐old P. abies and 321 four‐year‐old P. sylvestris plants were inoculated and the extent of infection determined 16 weeks later. H. annosum s.s. grew further than H. parviporum in P. sylvestris sapwood, while in P. abies, no differences between the two Heterobasidion spp. were found. Both H. annosum s.s. and H. parviporum spread faster in the sapwood of P. abies than in P. sylvestris. There was high within‐host species variation in growth rates for both P. sylvestris and P. abies suggesting it may be possible to identify tree genotypes with lower susceptibility.     

Influence of severe drought on the resistance of Pinus yunnanensis to a bark beetle‐associated fungus

Research on tree response to pest attacks under drought and heat stress is crucial for predicting the effect of climate change on forest pests and tree health. In this work, we studied the influence of severe water stress on the resistance of Pinus yunnanensis to inoculations of Grosmannia yunnanensis, a pathogenic fungus associated with the aggressive bark beetle, Tomicus yunnanensis. Experiments were performed in two plots, one located at the top of a hill and the other at the foot of a hill, in Xiaojiu, Yunnan, China, from May to September 2010 and March to April 2012. Measurements of soil and needle water content and predawn needle water potentials confirmed that severe droughts occurred during these periods. Maximum water stress intensity even occurred in 2010 during the typical rainy season. Following low‐density inoculations, the reaction zone length and fungal growth were measured in the phloem. Sapwood blue staining and total sapwood occlusion were quantified following fungal mass inoculations. Our results suggest that severe water stress has a negative impact on a tree's resistance to G. yunnanensis. By comparing our results to previous work performed from 1997 to 1999 on the same tree species, and in the same locality under mild water stress, we concluded that drought had opposite effects on tree resistance above and below a certain threshold of predawn needle water potential. The threshold, corresponded to maximum efficiency for tree defence mechanisms, was visible in our results, and was estimated to be approximately ‐1.1 MPa to ‐1.2 MPa for P. yunnanensis under local conditions. We suggest that the existence of such a threshold of water stress intensity may be viable for any conifer undergoing biotic aggressions and, specifically, bark beetle attacks.     

Fungi associated with Cyclaneusma needle cast in Scots pine in the west of Poland

Needles of Pinus sylvestris with and without symptoms of Cyclaneusma needle cast, from the west of Poland, were examined for abundance and diversity of fungi using Illumina sequencing. Fungal communities were dominated by Ascomycota (93.6%–98.6% of OTUs). Basidiomycota and non‐culturable fungi were less frequent. Needles were colonized by 260 taxa. Ascomycota, Basidiomycota and Glomeromycota were represented by 149, 39 and 1 taxa. Abundance of fungi was least in 1.5‐year‐old needles attached to twigs and greatest in fallen 2‐year‐old needles. Fungal communities had least diversity in 1.5‐year‐old needles and most diversity in 0.5‐year‐old needles of current growth. It was found that (a) the most common fungi were the needle pathogens Cyclaneusma minus, Lophodermium spp. and Sydowia polyspora; (b) less common potential pathogens were Cenangium ferruginosum, Coniothyrium complex, Desmazierella acicola, Neocatenulostroma germanicum and species in the genera Neodidymelliopsis, Pestalotiopsis, Phoma, Pleurophoma and Pyrenochaeta; (c) common primary or secondary saprotrophs included species of Alternaria, Aureobasidium, Beauveria, Cladophialophora, Cladosporium, Epicoccum, Exophiala, Lecanicillium, Penicillium, Cryptococcus and Kwoniella; (d) Lophodermium was represented mostly by Lophodermium pinastri which occurred 4–72 times more frequently than Lophodermium seditiosum; (e) frequencies of C. minus and C. ferruginosum were lower in the 0.5‐year‐old symptomless needles, increased in the symptomatic and symptomless 1.5‐year‐old needles and decreased after needle fall; (f) frequency of L. seditiosum was highest in 0.5‐year‐old needles; (g) frequency of L. pinastri increased with needle age whereas S. polyspora increased after needle fall; (h) lower frequency of L. pinastrii was associated with higher frequency of S. polyspora. It was concluded that Cyclaneusa needle cast in Poland may be caused by C. minus accompanied by C. ferruginosum, L. seditiosum, L. pinastrii and S. polyspora. Participation of Coniothyrium spp., Epicoccum nigrum, Pestalotiopsis spp. and Phoma spp. in the disease progress cannot be excluded.     

Mycelial growth and exclusion of Heterobasidion parviporum inoculated in branches of 15‐year‐old Picea abies clones

Twigs of 22 clones of 15‐year‐old Picea abies grafts were inoculated with Heterobasidion parviporum in July and in September 2003. Fungal growth varied between clones and exclusion of the pathogen varied significantly among clones inoculated in July. The results indicate that twigs exhibit the same infection pattern as cuttings when inoculated with H. parviporum and that exclusion of the pathogen in twigs is a clone‐dependent character that occurs during the vegetation period.     

Effects of wide spacing and thinning strategies on wood quality in Norway spruce (Picea abies) stands in southern Sweden

Abstract

The initial density of a stand influences both the prethinning growth and the quality of the harvested trees. This study investigated the effects of different square spacings (2.0, 2.5 and 3.0 m) with thinning from above and thinning from below on stand development and tree characteristics in a 33-year-old Norway spruce [Picea abies (L.) Karst.] plantation in southern Sweden. Before thinning the total standing volume was not significantly different between treatments. Diameter at breast height (dbh) and diameter of the thickest branch were positively correlated. Before thinning, dbh of the trees and their thickest branches were significantly higher in the stands with 3.0 m spacing. After thinning, the dbh and the diameter of the thickest branch did not significantly differ between the 3.0 m spacing with thinning from above and 2.0 and 2.5 m spacing with thinning from below. Spacing did not significantly influence the presence or size of spike knots. The results suggest that a combination of wide spacing with thinning from above may yield timber of similar quality to denser spacing with thinning from below.     

Age-related effects on leaf area/sapwood area relationships,canopy transpiration and carbon gain of Norway spruce stands (Picea abies) in the Fichtelgebirge,Germany

Stand age is an important structural determinant of canopy transpiration (E(c)) and carbon gain. Another more functional parameter of forest structure is the leaf area/sapwood area relationship, A(L)/A(S), which changes with site conditions and has been used to estimate leaf area index of forest canopies. The interpretation of age-related changes in A(L)/A(S) and the question of how A(L)/A(S) is related to forest functions are of current interest because they may help to explain forest canopy fluxes and growth. We conducted studies in mature stands of Picea abies (L.) Karst. varying in age from 40 to 140 years, in tree density from 1680 to 320 trees ha(-1), and in tree height from 15 to 30 m. Structural parameters were measured by biomass harvests of individual trees and stand biometry. We estimated E(c) from scaled-up xylem sap flux of trees, and canopy-level fluxes were predicted by a three-dimensional microclimate and gas exchange model (STANDFLUX). In contrast to pine species, A(L)/A(S) of P. abies increased with stand age from 0.26 to 0.48 m(2) cm(-2). Agreement between E(c) derived from scaled-up sap flux and modeled canopy transpiration was obtained with the same parameterization of needle physiology independent of stand age. Reduced light interception per leaf area and, as a consequence, reductions in net canopy photosynthesis (A(c)), canopy conductance (g(c)) and E(c) were predicted by the model in the older stands. Seasonal water-use efficiency (WUE = A(c)/E(c)), derived from scaled-up sap flux and stem growth as well as from model simulation, declined with increasing A(L)/A(S) and stand age. Based on the different behavior of age-related A(L)/A(S) in Norway spruce stands compared with other tree species, we conclude that WUE rather than A(L)/A(S) could represent a common age-related property of all species. We also conclude that, in addition to hydraulic limitations reducing carbon gain in old stands, a functional change in A(L)/A(S) that is related to reduced light interception per leaf area provides another potential explanation for reduced carbon gain in old stands of P. abies, even when hydraulic constraints increase in response to changes in canopy architecture and aging.     

Ophiostomatoid fungi associated with root‐feeding bark beetles on Scots pine in Poland

Ophiostomatoid fungi are known to be associated with various species of bark beetles. However, information about fungal associates of root‐feeding bark beetles in Europe is still fragmentary. For this reason, the fungal associates of Hylastes ater, H. opacus and Hylurgus ligniperda on Pinus sylvestris were isolated and identified. A total of 743 fungal isolates were collected and separated into 10 morphological groups. Analyses of ITS rDNA and partial β‐tubulin gene sequences confirmed that these groups represented distinct species. The 10 species included a total of 13 associations between fungi and bark beetles that had not been recorded previously. All of the bark beetles examined were frequently associated with ophiostomatoid fungi. The fungal diversity and relative abundance of species were very similar in the three species of root‐feeding bark beetles. The most commonly encountered associates of these beetles were Grosmannia radiaticola, Leptographium lundbergii, L. procerum and L. truncatum. Insect infestation data furthermore suggest that Hylastes spp. and Hg. ligniperda are also important vectors of the fungal pathogen Sphaeropsis sapinea.     

Frequency, species composition and efficiency of Ips typographus (Col., Scolytidae) parasitoids in infested spruce forests in the National Park “Bavarian Forest” over three consecutive years

During the summers of three consecutive years (2002, 2003 and 2004) the parasitoid fauna of the spruce bark beetle Ips typographus was investigated in the national park “Bavarian Forest”. In the central part of this forest no human influence in the population dynamics is allowed, whereas, in the surrounding no bark beetle attacks are accepted and all infested wood is removed consequently. Species frequency and species composition did not differ much in 2002 and 2003, when Coeloides bostrichorum and Roptrocerus sp. was most numerous. But in 2004 species composition changed with the increase of R. tutela and the decrease of C. bostrichorum. We found that C. bostrichorum reached very high numbers of individuals, but its frequency did not exceed 31% during 3 years while the pteromalid wasps were not so numerous, but had very high frequencies. For Roptrocerus, we found 55, 82 and 85% and for R. tutela 41, 67 and 85% frequency. In 2004, mean parasitization was higher (8.5) as in 2003 (5.8%). The highest parasitization in one sample was 92.2% in 2002 caused by C. bostrichorum, 73.5% in 2003 caused by C. bostrichorum and R. tutela and 59.8% in 2004 caused by R. tutela and Roptrocerus. Our hypothesis that the influence of parasitoids on the population dynamics of I. typographus is greater in natural forests than in normal treated forests could not be corroborated.     

Diversity of ophiostomatoid fungi associated with the large pine weevil, Hylobius abietis, and infested Scots pine seedlings in Poland

Context

Bark beetles are known to be associated with fungi, especially the ophiostomatoid fungi. However, very little is known about role of pine weevils, e.g., Hylobius abietis, as a vector of these fungi in Europe.

Aims

The aims of our study were to demonstrate the effectiveness of H. abietis as a vector of ophiostomatoid fungi in Poland and to identify these fungi in Scots pine seedlings damaged by weevil maturation feeding.

Methods

Insects and damaged Scots pine seedlings were collected from 21 reforestation sites in Poland. The fungi were identified based on morphology, DNA sequence comparisons for two gene regions (ITS, β-tubulin) and phylogenetic analyses.

Results

Sixteen of the ophiostomatoid species were isolated and identified. In all insect populations, Leptographium procerum was the most commonly isolated fungus (84 %). Ophiostoma quercus was also found at a relatively high frequency (16 %). Other ophiostomatoid fungi were found only rarely. Among these rarer fungi, four species, Leptographium lundbergii, Ophiostoma floccosum, Ophiostoma piliferum and Sporothrix inflata, were isolated above 3 %. L. procerum was isolated most frequently and was found in 88 % of the damaged seedlings. S. inflata was isolated from 26 %, while O. quercus occurred in 10 % of the seedlings.

Conclusion

This study confirmed that L. procerum and O. quercus were common associates of H. abietis, while others species were found inconsistently and in low numbers, indicating causal associations. H. abietis also acted as an effective vector transmitting ophiostomatoid species, especially L. procerum and S. inflata, to Scots pine seedlings.