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Article

Frost Cracks Show a Slight Effect on Fungal Richness in Stem Wood of Hybrid Aspen Trees in Latvia

by
Dārta Kļaviņa
*,
Roberts Matisons
,
Annija Auniņa
,
Zane Striķe
,
Laima Ciseļonoka
,
Keitlīna Krastiņa
,
Mārtiņš Zeps
,
Āris Jansons
,
Krišs Bitenieks
,
Dainis Edgars Ruņģis
and
Tālis Gaitnieks
Latvian State Forest Research Institute Silava, Rigas 111, LV-2169 Salaspils, Latvia
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(1), 14; https://doi.org/10.3390/d16010014
Submission received: 23 November 2023 / Revised: 18 December 2023 / Accepted: 22 December 2023 / Published: 25 December 2023
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Abstract

:
Hybrid aspen Populus tremula L. × Populus tremuloides Michx. is fast-growing and a potential source of biomass for bioenergy production in Europe. However, knowledge about the phytopathological risks to hybrid aspen clones, particularly about frost crack damage as a possible infection gateway of fungal infections, is scarce. Five clones, represented by 205 trees from three trials in Latvia, were studied; two wood samples (at root collar and 1.3 m height) were obtained from each tree. Wood-inhabiting fungi were isolated and identified by the morphology and sequencing of the ITS region with fungal-specific primers, and fungal communities were compared using PERMANOVA. Fungal communities from trees with stem cracks were richer in species, especially pathogens, and species richness was higher in samples collected at 1.3 m height. Plant pathogens were isolated from 52% of all samples. Soft rot-causing Alternaria and Fusarium were dominant; Alternaria was more common at the height of 1.3 m, while Fusarium was more common at the root collar. White rot fungi were isolated from less than 2% of all samples, indicating a low degree of tree infection in the 15- to 16-year-old plantations. Clonal differences were not significant for fungal communities in general; nevertheless, for the occurrence of the genus Cladosporium, clonal differences were observed. In conclusion, the differences in fungal communities in relation to stem cracks implied only indirect clonal effects on phytopathological risks, emphasizing the resistance to stem cracking as a crucial trait for the sustainability of hybrid aspen plantations.

1. Introduction

Afforestation with deciduous trees, specifically on abandoned agricultural lands, is highly recommended in Europe to increase carbon sequestration and to contribute to biotechnological development in wood product industries while meeting the growing demand for forest products [1]. Hybrid aspen (Populus tremula L. × P. tremuloides Michx.) is among the most promising alternatives due to high biomass production and climatic tolerance [1,2]. The number of monocultural hybrid aspen plantations is increasing in Northern Europe [3], and it can potentially help achieve various forestry objectives [1,2,3]. Climate hardiness is an important aspect of clone selection for breeding, and in particular, frost crack formation is a common occurrence [2,4,5]. The low wood density of hybrid aspens, particularly when ramets are young (less than 10 years), facilitates frost cracking as trees grow older [6,7]. Bark wounds can serve as a gateway for fungal infections, which reduce timber quality and stored carbon, thus affecting field performance and sustainability of stands, e.g., [8,9,10,11,12]. Nevertheless, studies on the occurrence and pathogenicity of fungi in hybrid aspen stand in association with frost cracks are very limited despite the high occurrence of frost cracks [5].
Heart rot is common for aspens and is caused mainly by basidiomycetes; thus, wood decay frequency increases with tree age [13,14]. Prior basidiomycetes wood of aspens is often colonized by anamorphic ascomycetes, causing wood straining as an initiation of decay [13,14]. Additionally, several types of cankers have been described as aggressive and causing extensive infection in various Populus species [2,15,16], and outbreaks have been reported in the Baltic States and Fennoscandia [1,17,18,19]. Knowledge about wood-inhabiting fungal communities is important for analysis of their interactions in wood to model, control, and predict decay and pathogenicity [20,21,22]. Although hybrid aspen is more resistant to disease compared to the parent species, susceptibility to fungal pathogens varies among clones [2,5,23,24]. Accordingly, wood-inhabiting fungi in hybrid aspen wood could be clone specific, and knowledge about fungal communities could be advantageous for maximization of yield, e.g., [25].
This study identified wood-inhabiting fungal communities in hybrid aspen clones and analyzed them in relation to frost cracks as a potential gateway of infection. We hypothesized that pathogen infection would be facilitated by the presence of frost cracks, but that the fungal communities would be clone-specific.

2. Materials and Methods

2.1. Sampling

Three trials of aspen hybrid clones established in 2005–2006 on former agricultural lands in the central part of Latvia (56°27′ N, 22°53′ E) with flat topography and well-drained arenosols were sampled. The soil was plowed before the establishment of the trials. Hybrid aspen clones were obtained by controlled crossings of the American aspen Populus tremuloides Michx (from the National Botanical Garden in the central part of Latvia) with plus trees of local common aspen Populus tremula L. [24]. The clonal composition of the trials was not completely overlapping. The planting material was one-year-old containerized plantlets, which were produced by a microclonal propagation method. Two trials (No. 640 and No. 699) had a block plot design, with 25 trees (5 × 5) in a block replicated six times (trial No. 640) and 16 trees in a block (4 × 4) replicated four times (trial no. 699). Trial No. 620 had single tree plots with 25 randomly distributed trees per clone. Tree spacing was similar in all trials, with the plantlets aligned according to a 3 m × 3 m grid. The first thinning was conducted in the year 2020, harvesting approximately half of the trees. According to an inventory in 2013 and 2020, the studied trials had a high occurrence of trees with stem frost cracks, which had likely formed in the winter of 2012/2013; hence, their age was approximately 10 years old; their length range was 5–85 cm [5].
To evaluate wood-inhabiting fungal communities, five clones (No. 4, 36, 41, 43, 44) were selected. These clones had intermediate productivity and occurrence of stem cracks in comparison to the trial means but had a relatively high incidence of stem rot [5]. In two of the trials (No. 640 and 699), 18 trees per clone were sampled (six trees per clone from three block plots), resulting in 90 trees per trial in total. In trial No. 620, only clone No. 4 among the selected was represented, from which all 25 trees were sampled.
To account for vertical differences in the distribution of wood rot [26] and hence fungal communities within stems, two increment cores per tree, one at breast height (approximately 1.3 m above the ground) and another at the root collar height (approximately 0.3 m above the ground) were collected using 5.15 mm increment corer in 2022. Samples were taken from the south-facing part of the stem; the corer was surface-sterilized using 70% ethanol for each sample. It was ensured that all samples contained pith. A total of 410 wood samples from 205 trees were obtained. For the sampled trees, dimensions were measured, and the presence of stem cracks was recorded.

2.2. Isolation and Identification

Each tree core without the bark layer was split into approx. 8 cm long pieces, and, after sterilization by flame, each piece was individually placed in a 9 cm plastic Petri dish with Hagem agar media (5 g glucose, 0.5 g NH4NO3, 0.5 g MgSO4 7H2O, 5 g malt extract, 20 g agar, 1000 mL distilled H2O at pH 5.5) and incubated at room temperature [9,10,12,27]. Plated cores were examined every three days, and all morphologically distinct fungi were isolated to pure cultures. Fungal cultures were identified or sorted by their growth morphologies using a Leica DM 4000B (100× magnitude) microscope (Leica, Wetzlar, Germany). Considering that Basidiomycetes and Ascomycetes may not form characteristic structures (e.g., conidia) under the laboratory conditions, thus being morphologically unidentifiable, fungal ITS region sequencing, which is a universal method, was used for the identification [10,12,28,29]. The mycelium of a representative isolate of each unidentified morphotype was collected from the surface of the media by a sterilized scalpel and stored in a 2 mL Eppendorf tube for molecular identification. The DNA isolation was performed using a modified CTAB extraction [12,27] and for fungal DNA amplification, ITS1F (5′-CTTGGTCATTTAGAGGAAGTAA-3′) and ITS4 (5′-TCCTCCGCTTATTGATATGC-3′) primers were used, which provides almost full ITS region sequencing and consequently longer reads than primers aiming only part of this region [28,29]. Amplicons were Sanger sequenced [30] in one direction using the ITS4 primer either at Macrogen Europe, Amsterdam, The Netherlands, or at the LSFRI Silava Genetic Resource Centre. The nucleotide sequences were analyzed using the BLAST function in the UNITE and NCBI platforms [31,32]. The criteria to assign taxonomy for representative sequences was BLAST values for family-level > 85%, genera-level > 90%, and species-level > 97%. Taxa falling below these thresholds were considered unidentified fungi at particular taxonomic levels. To assign functions and ecology (primary lifestyle) to each fungal genus, we used the FungalTraits database [33].

2.3. Data Analysis

To assess the determinants of the fungal richness in stem wood of hybrid aspen, generalized linear mixed-effects models (glmer) were used for the number of taxa according to general ecological traits (plant pathogens and saprotrophs), as well as all taxa. A Poisson distribution with a log link function was used for the generalization. The general form of the models was as follows: l o g E T = β 0 + β 1 H p + β 2   K + β 3 H + β 4 D + β 5 P + u E x , P a r , T r e e , where l o g E T represents the logarithm of the expected values for the taxon group (all taxon or particular trophic (ecological) groups of plant pathogens and saprotrophs), and β 0 ,   β 1 ,   β 2 ,   β 3 , β 4 ,   β 5 are regression coefficients associated with the variables: sampling height (Hp; categorical, two levels), clone (K; categorical, five levels), tree height (H; numeric), tree diameter (D; numeric), and bark crack presence (P; binomial). The term u ( E x ,   P a r ,   T r e e ) represents the random effect of the tree (Tree; specific ID of each tree) nested in replication (Par; subplot or replication block) nested within trial (Ex; categorical, three levels). Similar models were used to assess the effects of the above-mentioned determinants on the occurrence (binomial) of fungal genera represented in at least 15% of the samples. In these cases, a binomial distribution with a logit link function was used for generalization. The type II Wald Chi-square test was used to assess the significance of the fixed effects [34].
As a proxy for fungal beta diversity, the Shannon diversity index-based [35] distance matrix of dominant genera (represented in more than 1% of samples) built by function distance phyloseq package was used [36]. To infer variables affecting the diversity of fungi in wood samples, we performed Permutational Multivariate Analysis of Variance Using Distance Matrices (PERMANOVA) using the adonis2 function (999 permutations) of the vegan package [37]. In the PERMANOVA analysis, effects of sampling height, clones, and trials were tested simultaneously, thus disentangling their contributions. Predictors were tested for collinearity using the vif function from the car package [34]. The significance of differences between the levels of significant factorial predictors was estimated using the function pairwiseAdonis [38]. Data analysis was performed using version 4.3.0 of the R software [39] with the packages vegan [37], gplots [40], lme4 [41], car [34], and phyloseq [36].

3. Results

The analyzed samples contained abundant fungal mycelia and a total of 831 fungal cultures were isolated from the 410 analyzed wood cores. The majority of the cultures (667 isolates, 80% of the total) were obtained from samples collected at the height of 1.3 m. Isolates were morphologically diverse, and 80 morphotypes were identified, most of which belonged to Ascomycetes. The majority of the morphotypes (77) were identified at the species level, while the remaining were identified at the genus level (Table S1). In total, 56 fungal genera were identified, and 20 of them were isolated from more than 1% of the samples (Table 1). Fungal communities were dominated by Trichoderma, Penicillium, Alternaria, Cladosporium, and Fusarium genera, which were present in more than 30% of the trees sampled (Table 1).
Plant pathogens were the most abundant functional groups (Table 2), represented by 21 taxa, with two genera causing soft rot Alternaria spp. and Fusarium spp., being the most abundant and isolated from 40% and 35% of trees, respectively (Table 1). White rot-causing genera were considerably less abundant and were represented by Chondrostereum, Peniophora, and Hypholoma; only Chondrostereum was found in more than 1% of all sampled trees. The genus Ophiostoma spp., which causes wood discoloration, was isolated from 18 trees, particularly from samples collected at the height of 1.3 m.
Saprotrophs were the second most abundant functional group, among which litter and unspecified saprotrophs were the most frequent (Table 2). The litter saprotrophs were dominated by the genera Cladosporium and Cadophora, while Penicillium was the most common genus of the unspecified saprotrophs (Table 1). Considering that the analyzed trees were young, wood saprotrophs were less abundant and were detected in 20% of analyzed trees. Interestingly, the most abundant fungi of this group Ascocoryne spp. and Physalospora spp. were mainly isolated at 1.3 m height (17 out of 18 samples for Ascocoryne and all 12 samples for Physalospora).
The tested fixed effects had a low impact on the richness of taxa of wood-inhabiting fungi, except for sampling height, which indicated an explicit vertical fungal distribution pattern for both pathogens and saprotrophs (Table 3). Most of the taxa (77 taxa, 96%) were present at the 1.3 m height, while only 10 (13%) were detected at the stem base. The presence of frost cracks had a significant (p < 0.05) but weaker effect on the total fungal richness and the richness of plant pathogens, but not saprotrophs (Table 3). Clone and tree dimensions did not have a significant effect on the richness of fungal taxa.
Similarly, the analysis of the occurrence of dominant fungal genera revealed a strong vertical distribution pattern: Alternaria spp., Penicillium spp., and Trichoderma spp. were more commonly isolated from samples collected at a height of 1.3 m compared to 0.3 m (32% vs. 12%, 38% vs. 12% and 34% vs. 24%, respectively), while Fusarium spp. showed the opposite trend—lower occurrence in samples collected at 1.3 m in comparison to root collar samples (12% and 27%, respectively) (Table 4). Furthermore, for the genus Cladosporium, clonal differences among trees were significant (χ2—9.77; p < 0.05) (Table 4). Cladosporium was more frequent in hybrid aspen clones no. 43 and 44.
Fungal diversity represented by the Shannon diversity distance matrix was similar among samples and did not show any correspondence to clonal differences; sampling height and experimental trial were significant predictors for the fungal communities (Table 5). Shannon diversity differed significantly between trial no. 640 and 699 (p < 0.05). Fungal communities at the root collar and breast height were largely overlapping, and the majority of genera are common between groups and closely associated (Figure 1).

4. Discussion

Trees previously exposed to pathogens might have developed resistance, thus making them less susceptible to specific diseases [42], and trees previously colonized by less aggressive species can result in higher susceptibility to more competitive pathogens [43]. Therefore, due to genetic variation, different clones may have differing levels of resistance to fungal pathogens [2]. However, the analyzed hybrid aspen clones had generally similar wood-inhabiting fungal communities, with similar fungal richness and overlapping occurrence of the majority of fungal genera, implying variation of fungi resistance among analyzed clones. The lack of differences might be due to the limited set of clones analyzed as well as the stratified selection. Nevertheless, fungal competition and micro-environmental differences in soil moisture and nutrient availability create slightly different growing conditions for individual trees and can have a strong impact on fungal communities present in the wood [44,45]. Accordingly, PERMANOVA analysis (Table 5) identified site effect as significant for the dominant fungal community, and it had a higher impact than clonal differences. The occurrence of taxa and ecological groups (Table 1) suggested two possible cases of inhibiting fungal interaction. The contrasting occurrence of common aspen pathogens canker-causing ascomycetes Hypoxylon spp. [15,16] and Epicoccum spp. supported inhibitory interspecies relationship [46,47,48,49,50]. In the second case, the aspen stem rot agent Phellinus tremulae, i.e., [51] which is highly common and expected on aspens, was absent, but its antagonist, the rot-causing basidiomycete Peniophora polygonia ([52] and references therein), was found.
Fungal communities were dominated by two plant pathogen genera of Ascomycetes genera (Figure 1), which are common on trees at a young age [45]. Accordingly, rot-causing basidiomycetes that develop with tree age were substantially less frequent [53]. Nevertheless, different methodological approaches, such as direct sequencing from wood samples, could have resulted in a higher occurrence of Basidiomycetes which could be present in the wood but develop slower than Ascomycetes on agar media [22]. The main genera are known to cause moderate, non-fatal damage: Alternaria generally causes crown diseases of aspen infecting leaves and branches, and Fusarium spp. infection symptoms include the yellowing and wilting of leaves, cankers, and necrosis [54,55,56,57,58]. Accordingly, most represented genera belonged to weak pathogen groups that consequently have a low direct impact on timber quality. Still, the Ascomycete genus Trichoderma, which has a principally mycoparasitic lifestyle, was commonly found in our data set. This could indicate some wood decay processes as it has the potential to cause soft rot [33] and can enter the wood tissues through natural openings or wounds, mainly in the roots [59,60].
Some clonal effect was detected for the fungal genus Cladosporium, which generally has a saprotrophic lifestyle but may be present in plant tissues as an endophyte or even a pathogen [61] (Table 4). The capacity for Cladosporium species to act as hyperparasites of poplar leaf rust disease-causing fungi has been suggested [62,63], and the interactions of these fungi in the context of poplar selection for pathogen resistance have been shown [63]. Therefore, as a further task, a wider screening of hybrid aspen clones for Cladosporium occurrence could be performed, combining this knowledge with clone resistance to leaf rust infection [62,63].
Frost crack incidence had a positive effect on the total number of fungal taxa, particularly plant pathogens (Table 3), implying a higher risk for wood quality and timber production as a consequence, e.g., [8,9,10,11,12]. Furthermore, such a relationship indicates an indirect effect of hybrid selection, as frost crack frequency in hybrid aspen has clonal differences [5,64]. Additionally, vertical differences in fungal communities and their diversity emphasize stem bark injuries (due to frost cracks or other damage) as the main entry point for pathogens [65].
Although none of the detected fungal genera directly corresponded to frost crack incidence or presence (Table 4), the ecology of several of the detected taxa is closely related to frost crack or other bark injuries [66,67,68]. Regarding Fusarium spp., one of the dominant plant pathogens in our data set, several studies have found associations between Fusarium canker development in aspens and bark wounds, such as pruning wounds, frost cracks, insect damage, and even beaver feeding ([69] and references therein). Åström and Ramstedt (1994) [66] reported it as a secondary pathogen on frost crack-affected willows, suggesting that it can contribute to canker or other stem disease development that could lead to reduced wood quality. Other genera observed at a low frequency also indicated some connection to bark damage: Didymella, Apiospora, and Ascocoryne. Blue-strain fungus Ophiostoma spp. enters wood through frost cracks [67,70,71,72]; Phoma herbarum has been reported to cause stem cankers via bark wounds and injuries as entry points [66,68,73]. Lastly, frost cracks could have contributed to the establishment of the infection of Chondrostereum purpureum, the most abundant white rot-causing basidiomycete in our data set, as bark lesions and other mechanical damage contribute to infection with this fungus [74,75]. However, it must be acknowledged that the interpretation was based on the most common ecological groups of genera, which can contain species of different ecology [33,61]; hence, functional diversity might be underestimated. Also, some specific taxa might be under-represented due to the application of cultivation media, although Hagem agar media is a selective media particularly aimed at slow-growing wood-inhabiting fungi [27].
The low occurrence of direct decay and rot-causing wood pathogens and a high abundance of pathogenic ascomycetes, particularly in the case of frost cracks, indicated a weak but sable risk of stem canker formation, wood straining, or soft rot. As frost cracks were associated with clonal differences, breeding efforts to lower the incidence of cracking could decrease infection rate and potential pathogen frequency in the wood, thus contributing to the wood quality and prevention of the initiation of rot in the stem.

5. Conclusions

Fungal communities in the studied hybrid aspens were homogenous and mainly formed by weakly pathogenic Ascomycetes that can cause cankers, soft rot, or foliar or branch diseases. The presence of white-rot-causing fungi had a low frequency, indicating a low rot risk for young hybrid aspens. Frost cracks, the occurrence of which is clone specific, were related to a higher richness of wood inhabiting, especially pathogenic fungi; therefore, the selection of clones with a lower incidence of cracking is recommended. Lastly, the occurrence of Cladosporium spp. was detected to be clone specific, which could be considered for breeding purposes, as the genus has the potential for leaf rust biocontrol.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16010014/s1, Table S1: Identification of isolated fungi from hybrid aspen wood (taxa, sequence accession numbers in NCBI, Species Hypothesis and reference sequence, and corresponding Blast results (percentage of identity and Blast score).

Author Contributions

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

Funding

The research was funded by JSC Latvia’s State Forests, project “Assessment of future phytopathological risks” no. 5-5.9.1_007f_101_21_69, Latvian Science Council project no. lzp-2022/1-0283 “Role of mycorrhizal fungi in inter-plant signalling and pest tolerance of hybrid aspen and silver birch”, and ERDF project No 1.1.1.1/21/A/063 “Tool for assessment of carbon turnover and greenhouse gas fluxes in broadleaved tree stands with consideration of internal stem decay”.

Data Availability Statement

Data are available upon personal request to the corresponding author. Sequences are published in GenBank under Accession numbers OR636269-OR636303 and OR727911-OR727955.

Acknowledgments

The authors are grateful to Kaspars Polmanis, Natālija Burņeviča, Gints Jansons, and Reinis Vegners for their assistance in the field and lab work.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of this study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Diversity 16 00014 g001aDiversity 16 00014 g001b
Figure 1. Principal coordinate analysis (PCoA) plot with Shannon diversity for fungal communities. Sample (a) and fungal taxa (b) ordination are shown. Sampling height subgroups (RC—root collar and BH—1.3 m height) are indicated by color. Ellipses indicate 95% confidence intervals for those sample groups. First three letters for genera used as an abbreviation; full names of genera mapped are these: Fus—Fusarium; Neo—Neobulgaria; Tri—Trichoderma; Api—Apiospora; Asc—Ascocoryne; Aur—Aureobasidium; Epi—Epicoccum; Muc—Mucor; Cla—Cladosporium; Par—Paraconiothyrium; Pen—Penicillium; Per—Perconia; Phy—Physalospora; Cho—Chondrostereum; Alt—Alternaria.
Figure 1. Principal coordinate analysis (PCoA) plot with Shannon diversity for fungal communities. Sample (a) and fungal taxa (b) ordination are shown. Sampling height subgroups (RC—root collar and BH—1.3 m height) are indicated by color. Ellipses indicate 95% confidence intervals for those sample groups. First three letters for genera used as an abbreviation; full names of genera mapped are these: Fus—Fusarium; Neo—Neobulgaria; Tri—Trichoderma; Api—Apiospora; Asc—Ascocoryne; Aur—Aureobasidium; Epi—Epicoccum; Muc—Mucor; Cla—Cladosporium; Par—Paraconiothyrium; Pen—Penicillium; Per—Perconia; Phy—Physalospora; Cho—Chondrostereum; Alt—Alternaria.
Diversity 16 00014 g001aDiversity 16 00014 g001b
Table 1. Dominant fungal genera isolated from 15- to 16-year-old hybrid aspen wood.
Table 1. Dominant fungal genera isolated from 15- to 16-year-old hybrid aspen wood.
GenusPrimary Lifestyle *Relative Occurrence (%) and Number of Trees (in Brackets)
Trichodermamycoparasite49 (101)
Penicilliumunspecified saprotroph44 (91)
Alternariaplant pathogen40 (81)
Cladosporiumlitter saprotroph39 (80)
Fusariumplant pathogen35 (72)
Cadophoralitter saprotroph22 (46)
Didymellaplant pathogen20 (41)
Aureobasidiumsooty mold19 (39)
Phialocephalasoil saprotroph14 (30)
Epicoccumplant pathogen11 (24)
Ascocorynewood saprotroph9 (18)
Ophiostomaplant pathogen9 (18)
Paraconiothyriumsaprotroph7 (15)
Apiosporaplant pathogen7 (14)
Physalosporawood saprotroph6 (12)
Mucorsoil saprotroph5 (11)
Hypoxylonwood saprotroph3 (7)
Neobulgariawood saprotroph3 (6)
Chondrostereumplant pathogen3 (6)
Periconiaplant pathogen2 (5)
* based on Põlme et al. (2020) [33] classification.
Table 2. Distribution of wood-inhabiting fungal taxa based on the main functional groups (primary lifestyles) according to Põlme et al. (2020) [33] in 15- to 16-year-old hybrid aspen.
Table 2. Distribution of wood-inhabiting fungal taxa based on the main functional groups (primary lifestyles) according to Põlme et al. (2020) [33] in 15- to 16-year-old hybrid aspen.
Primary LifestyleRelative Occurrence (%) and Number of Trees (in Brackets)
Plant pathogens66 (135)
Litter saprotrophs56 (115)
Unspecified saprotrophs46 (95)
Mycoparasites34 (69)
Soil saprotrophs20 (42)
Wood saprotrophs20 (40)
Table 3. Strength (χ2 values) and significance (p-value) of the fixed effects of sampling height, presence of frost cracks, clone and tree dimensions) on the richness of fungal taxa inhabiting the wood of 15- to 16-year-old hybrid aspen in Latvia. For the random effects, variances are shown. Significance codes, p-values: *—<0.05; **—<0.001.
Table 3. Strength (χ2 values) and significance (p-value) of the fixed effects of sampling height, presence of frost cracks, clone and tree dimensions) on the richness of fungal taxa inhabiting the wood of 15- to 16-year-old hybrid aspen in Latvia. For the random effects, variances are shown. Significance codes, p-values: *—<0.05; **—<0.001.
Number of All Fungal TaxaNumber of Plant Pathogen TaxaNumber of Saprotroph Taxa
Fixed effect, χ2
Sampling height229.87 **38.29 **142.59 **
Presence/absence of frost cracks4.41 *5.38 *1.92
Clone4.320.615.14
Tree height0.030.010.18
Stem diameter0.630.000.05
Random effect, variance
Tree:(block:trial)6.00 × 10−106.54 × 10−90.00 × 100
Block: trial0.00 × 1000.00 × 1000.00 × 100
Trial3.29 × 10−32.06 × 10−20.05
Table 4. Strength (χ2 values) and significance (p-value) of the fixed effects of sampling height, presence of frost cracks, clone and tree dimensions) on the presence/absence of dominant wood-inhabiting fungal genera (Alternaria, Fusarium, Cladosporium, Trichoderma, and Penicillium) of 15- to 16-year-old hybrid aspen in Latvia. For the random effects, variances are shown. Significance codes, p-values: *—<0.05; **—<0.001.
Table 4. Strength (χ2 values) and significance (p-value) of the fixed effects of sampling height, presence of frost cracks, clone and tree dimensions) on the presence/absence of dominant wood-inhabiting fungal genera (Alternaria, Fusarium, Cladosporium, Trichoderma, and Penicillium) of 15- to 16-year-old hybrid aspen in Latvia. For the random effects, variances are shown. Significance codes, p-values: *—<0.05; **—<0.001.
AlternariaFusariumCladosporiumTrichodermaPenicillium
Fixed effect, χ2
Sampling height20.54 **14.97 **0.005.86 *25.77 **
Presence/absence of frost cracks2.390.830.710.050.83
Clone2.191.659.77 *0.857.86
Tree height0.800.030.000.410.00
Tree diameter0.060.480.050.202.85
Random effect, variance
Tree: (block:trial)5.06 × 10−54.24 × 10−73.01 × 10−72.74 × 10−61.11 × 10−1
Block: trial4.12 × 10−13.70 × 10−12.85 × 10−33.94 × 10−12.95 × 10−5
Trial3.47 × 10−21.02 × 10−12.80 × 10−13.22 × 10−22.87 × 10−7
Table 5. PERMANOVA summary for a model of the dominant fungal community (presence/absence data) according to sampling height, hybrid aspen clone, and experimental trial. Significance codes, p-values: *—<0.01; **—<0.001.
Table 5. PERMANOVA summary for a model of the dominant fungal community (presence/absence data) according to sampling height, hybrid aspen clone, and experimental trial. Significance codes, p-values: *—<0.01; **—<0.001.
FactorDegree of Freedom Sequential Sums of SquaresF StatisticsPartial R-Square ValuesPartial p-Values
Sampling height12.47423.6260.0540.001 **
Clone40.311 0.7420.0070.714
Trial20.5052.4120.0110.025 *
Residuals40242.104 0.925
Total40945.514 1.000
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Kļaviņa, D.; Matisons, R.; Auniņa, A.; Striķe, Z.; Ciseļonoka, L.; Krastiņa, K.; Zeps, M.; Jansons, Ā.; Bitenieks, K.; Ruņģis, D.E.; et al. Frost Cracks Show a Slight Effect on Fungal Richness in Stem Wood of Hybrid Aspen Trees in Latvia. Diversity 2024, 16, 14. https://doi.org/10.3390/d16010014

AMA Style

Kļaviņa D, Matisons R, Auniņa A, Striķe Z, Ciseļonoka L, Krastiņa K, Zeps M, Jansons Ā, Bitenieks K, Ruņģis DE, et al. Frost Cracks Show a Slight Effect on Fungal Richness in Stem Wood of Hybrid Aspen Trees in Latvia. Diversity. 2024; 16(1):14. https://doi.org/10.3390/d16010014

Chicago/Turabian Style

Kļaviņa, Dārta, Roberts Matisons, Annija Auniņa, Zane Striķe, Laima Ciseļonoka, Keitlīna Krastiņa, Mārtiņš Zeps, Āris Jansons, Krišs Bitenieks, Dainis Edgars Ruņģis, and et al. 2024. "Frost Cracks Show a Slight Effect on Fungal Richness in Stem Wood of Hybrid Aspen Trees in Latvia" Diversity 16, no. 1: 14. https://doi.org/10.3390/d16010014

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