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Article

Fungal Community Taxa Differ in Diversity and Number between Live and Dead Prunus serotina Ehrh. Wood in a Protected Forest within Its Secondary Range of Distribution

by
Marlena Baranowska
1,
Robert Korzeniewicz
1,
Jolanta Behnke-Borowczyk
1,
Wojciech Kowalkowski
1,
Dariusz Krupiński
2,
Andrzej Purcel
2 and
Adrian Łukowski
1,*
1
Faculty of Forestry and Wood Technology, Poznań University of Life Sciences, Wojska Polskiego 71c, 60-625 Poznan, Poland
2
Wielkopolski National Park, Jeziory, 62-050 Mosina, Poland
*
Author to whom correspondence should be addressed.
Forests 2023, 14(7), 1324; https://doi.org/10.3390/f14071324
Submission received: 16 May 2023 / Revised: 15 June 2023 / Accepted: 26 June 2023 / Published: 28 June 2023
(This article belongs to the Special Issue Fungi in Forest Ecosystems: Systematics, Diversity and Ecology)

Abstract

:
Prunus serotina is an important invasive plant species in Poland. It was introduced to European forests, even in places currently protected by law, such as national parks. One major factor contributing to the spread of this species is the lack of infecting pathogens and incomplete knowledge about the relationship between the plant and microorganisms. This study aimed to identify fungal communities collected from freshly cut stumps of live and dead black cherry tree specimens growing in a protected forest. The main working hypotheses were as follows: (i) fungal communities inhabiting the wood of dead and living trees will differ in diversity and the number of taxa; and (ii) saprotrophic fungi will dominate in the wood of dead tree stumps. This study applied Illumina sequencing based on the amplification of the fungal ribosomal ITSI region. The average number of sequences (OTU) obtained from the analysis of dead tree wood was 101,758, while that of living trees was 94,150. These sequences belonged to 312 taxa, among which 254 were isolated from the wood of dead trees and 171 from that of living trees. Among the saprotrophs on dead trees, the following species were identified: Stereum rugosum, Ganoderma adspersum, G. applanatum, Peniophora cinerea, and Ascocoryne cylichnium. On the other hand, in the wood of living trees, Cytospora leucostoma and Botrytis cinerea were the most abundant saprotrophic species. The fungal communities inhabiting the wood of dead and living trees differed in the diversity and abundance of taxa, thus confirming our hypothesis. The results of our research conducted in a protected area indicate that black cherry wood can be naturally colonized by many pathogen species that can further limit its expansion.

1. Introduction

Some species found outside the limits of their natural range spread intensively and spontaneously, thus gaining the status of invasive plants [1,2]. Together with non-native species [3], invasive species pose substantial threats to global and local biodiversity [4], and have a negative socio-economic and human health impact [5,6]. In forest ecosystems, such threats include hybridization, pathogen transmission, and species competition. Invasive species outperform native flora due to their faster growth, higher production capacity, more effective dispersal, higher tolerance to various environmental conditions, and fewer natural enemies, such as pathogens and herbivores [7]. Therefore, studying the role of plant–microbe/insect interactions—both antagonistic and synergistic—is essential for elucidating the mechanisms of the invasive plant species spread [8,9]. Plant invasion is also a major threat to forest biodiversity in protected areas [10,11].
More than 430 alien tree species worldwide are invasive species, and the list continues to grow as more tree species are moved around the world and thrive in new environments. According to Rejmánek and Richardson [12], 73 invasive alien tree species are found in Europe, 28 of which are used in forestry. The analysis of non-native species from the main European databases, DAISIE (www.europeliens.org, accessed on 1 April 2023) and EPPO [13], indicates that Prunus serotina Ehrh. (black cherry), Acacia dealbata L., Ailanthus altissima (Mill.) Swingle, and Robinia pseudoacacia L. are alien species particularly dangerous to native ecosystems. The dynamic development of the P. serotina population is most often observed in monocultures of Pinus sylvestris L. (Scots pine) or mixed stands with a large proportion of pine [14], in managed stands and stands under various forms of protection. Unfortunately, they are increasingly encroaching on the most fertile habitats of alder and riparian forests [15].
Reducing the occurrence of invasive species populations is essential to protecting native species [16]. However, regarding black cherry, no effective methods have been developed so far [17]. The current strategies used to reduce its occurrence include mechanical methods or their combination with a chemical (e.g., the Roztocze and Kampinoski National Parks in Poland) [18,19].
In Polish forests, restrictions are placed on chemical plant protection products [17], especially in protected areas (e.g., in national parks and nature reserves). An alternative could be the use of biological methods. Although wood pathogens can damage their hosts substantially, knowledge of the fungal pathogenic community and the mycobiome of Prunus wood is generally low, even regarding species native to Europe [20]. Black cherry wood is colonized by rich fungal communities, including taxa specializing in wood decay (saprotrophs) [21]. Interestingly, the use of the mycelium of Chondrostereum purpureum (Pers.) Pouzar was suggested to reduce the population of black cherry [22,23,24]. Few scientific reports refer to other fungi inhabiting the wood of black cherry. Black knot caused by Apiosporina morbosa (Schwein.) Arx, a widespread disease that can reduce timber value, can be identified on black cherry branches and stems [25]. Pathogens such as Armillaria spp. (Fr.) Staude, Cytospora leucostoma (Pers.) Sacc., Coniophora cerebella (Schumach.) P. Karst, Fomitopsis spraguei (Berk. & M.A. Curtis) Gilb. & Ryvarden, and Polyporus berkeleyi (Fr.) Bondartsev & Singer can also be found on black cherry trees and may be essential in limiting their spread [21]. Comprehensive studies of microscopic fungal communities inhabiting black cherry stumps have been conducted on the wood of P. serotina but only in managed pine stands, where this non-native plant had been previously controlled [26,27,28]. Macroscopic fungi associated with dead black cherry wood have been studied in the Kampinos National Park [18,29]. So far, no reports on the composition of fungal communities inhabiting black cherry stumps in stands not covered by standard forest management treatments are available.
Considering the above, this study aimed to identify fungal communities collected from freshly cut stumps of live and dead black cherry tree specimens growing in a protected area. The working hypotheses were as follows: (i) fungal communities inhabiting the wood of dead and living trees will differ in diversity and the number of taxa; (ii) saprotrophic fungi will dominate in the wood of dead tree stumps; and, (iii) we will be able to identify fungi that could potentially be proposed for the biological control of P. serotina. This study is part of a broader research concept searching for species potentially helpful for the biological control of black cherry. Fungal communities are analyzed to identify species causing stump decomposition that may inhibit the regrowth of black cherry trees, thus contributing to the effectiveness of an alternative method to control their spread by intentionally inoculating their stumps.

2. Materials and Methods

2.1. Field Works

The research was conducted in the Wielkopolski National Park (Poland) in the Wiry Protection District, where five research plots (approx. 0.25 ha each) were located in four forest divisions. The taxation description of the stands from which the research material was collected is included in Appendix A (Table A1). Black cherry was likely introduced artificially in this location years ago, as was usually done in Central and Eastern Europe. Black cherry trees were cut in the first half of August 2022 using a chain saw, standardizing the height of the stumps to 2.5–3 cm. The diameter of black cherry stumps ranged from 4 to 7 cm. The biological material (chips) was collected from the stumps of freshly cut black cherry trees (live and dead) using a cordless drill with 6 mm wood drill bits. To capture a representative sample from the largest area possible, wood samples were randomly collected from stumps of live (n = 25, five from each experimental plot) and dead trees (n = 25, five from each experimental plot). The five samples of dead or live trees from each experimental plot were combined into one sample (one combined dead sample and one combined live sample per plot). The combined dead or live tree samples from all five experiment plots (n = 5 for dead tree samples, n = 5 for live tree samples) were subjected to further analyses.

2.2. Laboratory Works

Wood chips collected from the field were ground in a PEXTM SamplePrepTM Freezer/MillTM cryogenic mill. A constant sample weight (1 g) was used for standardization. DNA was isolated using the Bead-Beat Micro AX Gravity kit (A&A Biotechnology, Gdynia, Poland) with an extended lysis step (up to 45 min). The metagenomic analysis of fungal communities was performed based on the ITS1 region. Specific primer sequences were used (ITS1FI2, 5′ GAA CCW GCGGAR TCA 3′; 5.8S, 5′ CGC TGC GTT CTT CATCG 3′) to amplify the selected region and prepare the library [30,31]. Each 25 μL PCR mixture included 0.2 μmol/L of each primer, 12.5 μL 2× PCR MIX (A&A Biotechnology, Gdynia, Poland), and 2 μL of total DNA extracted from the soil. The cycling conditions were as follows: 94 °C for 5 min, 35 cycles of 94 °C for 30 s, 56 °C for 30 s, and 72 °C for 30 s, and a final step at 72 °C for 7 min. The obtained DNA was purified using the Anti-Inhibitor Kit (A&A Biotechnology, Gdynia, Poland). The amplicons were sequenced using the Illumina system in the Genomed S.A (Warszawa, Poland). The PCR was performed using Q5 Hot Start High-Fidelity 2X Master Mix following the manufacturer’s instructions.
The sequencing was performed with a MiSeq sequencer in paired-end (PE) runs. The automatic pre-analysis of the data was performed on the MiSeq instrument using MiSeq Reporter (MSR) v2.6 software. Negative control samples were prepared and sequenced for each variant to remove artifacts generated during the analysis. The analysis comprised two stages: (1) automatic demultiplexing of samples; and (2) generation of fastq files containing raw readings. The obtained sequences were subjected to further bioinformatics analysis to prepare the OTU (operational taxonomic unit) library. Bioinformatics analysis ensuring the classification of reads to the species level was conducted with the QIIME2 software package (https://qiime2.org/, accessed 3 April 2023) based on the NCBI reference sequence database [32]. The analysis consisted in removing the adapter sequences in the cutadapt software (https://cutadapt.readthedocs.io/en/stable/, accessed 1 April 2023) [33] and then in the qualitative analysis of the reads. In the next step, paired sequences were combined (fastq–join algorithm) [34], and chimeric sequences were removed (usearch61 algorithm). Clustering was performed based on the selected reference sequence database (uclust algorithm), and taxonomy was assigned based on the NCBI reference sequence database (blast algorithm). The sequencing depth was set at 10,000, and its quality was confirmed by determining rarefaction curves [35].
For the species identification, the percentage of similarity between the analyzed sequence and the reference was assumed to be 98%–100% at the species level, 94%–97% at the genus level, and 80%–94% at the order level, with at least 90% overlap with the reference sequence. Communities were identified down to the lowest possible taxonomic level. OTUs that did not belong to Fungi or Oomycota were removed from further analysis. The function (trophic group) of individual taxa in the community was determined based on the FungalTraits database [36], and the applicable names were determined based on the Index Fungorum database (http://indexfungorum.org/, accessed on 2 April 2023).

2.3. Statistical Analysis

The obtained OTU library was compiled in an Excel spreadsheet and statistically analyzed using the R program [37]. Percentage data were transformed using a formula suggested by Bliss [38]. Before starting the statistical analysis of the results, the initial assumptions of the Shapiro–Wilk, Kolmogorov λ, and Bartlett’s tests were checked [39], and adonis2 function from the vegan package was used [40]. The Shapiro–Wilk test indicated that the noted data in this experiment were not normally distributed; therefore, they were log-transformed. Then, the results were checked with the Kolmogorov λ concordance test, which confirmed that the data did not have a normal log distribution. No datasets met the assumptions of ANOVA; thus, the Kruskal–Wallis (one-way test, χ2 approximation) was employed. The figures were generated using Microsoft Excel 2019 (Microsoft Corporation, 2019, Redmond, WA, USA).
Species biodiversity was determined for each community using diversity indices. Species richness was defined as the total number of species in the community, and frequency was defined as the percentage of a given taxon in the community. The Shannon diversity index (H’) was calculated. The dominance of a species in the fungal community was determined using the Berger–Parker dominance index in which the dominance of individual taxa in the community is deduced from the closeness of this value to unity. An NMDS analysis was conducted to illustrate differences between communities (NMDS, function metaMDS, vegan package; [40]. The results of the NMDS analysis, verified with a statistical ANOSIM test, were used to select indicator species of a given community.

3. Results

The OTU results indicated an average of 101,758 (SE = ±3781 SE) and 94,150 (SE = ±10,051) sequences after analyzing the dead and live wood, respectively, corresponding to 312 taxa (254 from dead trees and 171 from living trees). Among these communities, 141 taxa were common for the dead and living tree samples, 113 taxa occurred only in the dead trees, and 58 only in the living trees.
In the wood of the living trees, Ascomycota (77.8%), Mucoromycota (11.5%), Basidiomycota (8.0%), and Entorrhizomycota (2.4%) were the most numerous. Regarding the dead wood, the highest frequency was found in Basidiomycota (70.5%), Ascomycota (19.2%), and Mucoromycota (9.6%) (Figure 1). Statistically significant differences in the proportion of individual fungal classes between the live and dead individuals of black cherry were observed only for Ascomycota (p = 0.009) and Basidiomycota (p = 0.0122).
In the wood of the living trees, C. leucostoma, Diplodia sapinea (Fr.) P. Karst. and Penicillium canescens Sopp displayed the highest frequency, while Stereum rugosum Pers., Aspergillus parvulus G. Sm., and Ascocoryne cylichnium (Tul.) Korf were most frequent in the wood of the dead trees (Figure 2 and Table A2). The trophic group with the highest frequency in the tested samples were saprotrophs and plant pathogens observed in the wood of the dead trees (Figure 3). Among the saprotrophs, the following species were identified: S. rugosum, Ganoderma adspersum (Schulzer) Donk, G. applanatum (Pers.) Pat., Peniophora cinerea (Pers.) Cooke, and A. cylichnium. On the other hand, in the wood of the living trees, C. leucostoma and Botrytis cinerea (Pers.) were the most numerous pathogen species (Table A2).
Statistically significant diversity was observed regarding the saprotrophs. This group was analyzed to identify indicator species, including 268 taxa; indicator taxa for the living and dead trees were selected based on their presence in a given sample. In the first group, forty-nine were identified, and in the second group, only six were. In the community isolated from the wood of the living trees, the following were indicator species (p < 0.001): Absidia glauca Hagem, Allantophomopsis lycopodina (Höhn.) Carris, Alternaria axiaeriisporifera E.G. Simmons & C.F. Hill, A. hampshirensis Wanas., E.B.G. Jones & K.D. Hyde, A. infectoria E.G. Simmons, A. tenuissima (Kunze) Wiltshire, B. cinerea, Botrytis sp., Coniothyrium dispersellum P. Karst., C. pyrinum (Sacc.) J. Sheld, Didymella macropodii Petr., D. macrostoma (Mont.) Qian Chen & L. Cai, D. sapinea, D. seriata De Not., Dothiora prunorum (C. Dennis & Buhagiar) Crous, Epicoccum nigrum Link, Epicoccum sp., Fusarium avenaceum (Fr.) Sacc., Lewia infectoria (Fuckel) M.E. Barr & E.G. Simmons, Penicillium bialowiezense K.W. Zaleski, P. brevicompactum Dierckx, P. canescens, P. concentricum Samson, Stolk & Hadlok, P. scabrosum Frisvad, Samson & Stolk, P. soppii K.W. Zaleski, Pestalotiopsis sp., Phoma laundoniae Boerema & Gruyter, Phoma sp., Saitozyma podzolica (Babeva & Reshetova) Xin Zhan Liu, F.Y. Bai, M. Groenew. & Boekhout, and Stemphylium sp. The taxa most strongly associated with the wood of dead trees (p > 0.001) were the following: Talaromyces amestolkiae Yilmaz, Houbraken, Frisvad and Samson, S. rugosum, Collophora sp., and Phialocephala piceae (T.N. Sieber & Grünig) Rossman.
The results of the NMDS statistical analysis indicated differences between the fungal communities isolated from live and dead black cherry stump wood (Figure 4). Significant differences were found for the Shannon diversity and Berger-Parker dominance indexes between saprotrophic communities of dead and living trees (Figure 5). The value of the Shannon diversity index (p = 0.009) was higher for the community from living trees than that from dead trees. The Berger-Parker dominance index (p = 0.0003) was higher in dead trees than in live trees. These results confirmed the predominance of S. rugosum in the community.

4. Discussion

The results of this study indicated that the fungal communities of the living and dead trees differed, confirming our hypothesis. This difference was observed as early as the phylum level. Fungi from the Ascomycota phylum dominated the wood of the living black cherry individuals, while Basidiomycota dominated the wood of the dead trees. The dominance of Ascomycota in black cherry stumps has been demonstrated in previous studies [26,27,28]. The greater proportion of Basidiomycota in the wood of dead black cherry can be explained by its progressive decomposition. According to Kwaśna et al. [41], dead wood is a natural habitat for saprotrophic fungi, which explains the dominance of the latter in samples of dead wood.
The fungal communities inhabiting the wood of the dead and live black cherry trees differed in taxon diversity and abundance. Wood fungal communities associated with the live black cherry trees were more diverse, and more indicator species were selected for the living trees than for dead trees. The taxa most strongly associated with the wood of the dead trees while having a significant proportion in the fungal community were S. rugosum and P. piceae. S. rugosum (Basidiomycota) is a cosmopolitan pathogen, weakness parasite, and saprotroph, inhabiting mainly dead trunks and branches of deciduous trees [42]. Its fruiting bodies were observed on black cherry trunks during our research in the Wielkopolski National Park. In Poland, this species has already been isolated from black cherry wood [26], and the presence of its fruit bodies on P. serotina has been identified [29]. However, in the abovementioned studies, the proportion of this taxon in the studied community was lower. A significant proportion of S. rugosum in the analyzed fungal communities and the visible presence of its fruiting bodies in the study area (unpublished data) indicate that it can significantly affect the black cherry trees’ condition and health status. In addition to S. rugosum, other saprophyte species isolated from dead black cherry wood deserve more attention. The wood sample from plot I was dominated by Cordana pauciseptata Preuss (>50% proportion) and the sample from plot IV by A. cylichnium. Phialocephala piceae (Ascomycota) also had a significant proportion in the community of the dead wood fungi (Table A2). Until now, this species was considered an endophyte of coniferous needles [43], although other species of this genus have been isolated from black alder [44]. Its presence in the analyzed samples may result from the structure of the stand from which the samples were taken; the black cherry trees grew under the canopy of Scots pines. A similar situation may apply to D. sapinea (Sphaeropsis sapinea), which has been identified only in the wood of live black cherry trees. It is an endophyte, a pathogen causing the decline of coniferous species, in particular pines [45,46]. Further research should clarify the presence of these fungi in the tissues of deciduous trees.
On the other hand, the taxa most strongly associated with the wood of the living trees while having a significant proportion in the fungal community were B. cinerea, D. macrostoma, D. sapinea, D. prunorum, Epicoccum sp., F. avenaceum, P. bialowiezense, P. brevicompactum, P. canescens, P. laundoniae, and Stemphylium sp. Botrytis cinerea (Ascomycota) is a cosmopolitan and dangerous plant pathogen causing gray mold [47]. It can colonize plants internally (endophyte) without causing disease or stress symptoms [48]. The relationship between the presence of this fungus in generative organs and its presence in wood is unknown. Van Kan et al. [48] provided data on the occurrence of B. cinerea only in the generative organs of the woody plants Sorbus acuparia and Rubus fruticosa (Rosaceae) (B. A. P. Rajaguru, University of Reading, unpublished results). The presence of this fungus as an endophyte in black cherry tissues may indicate increased inbreeding and reduced genetic diversity in this area [48]. Prunus serotina trees in the Wielkopolski National Park displayed various signs of weakness. The symptoms of stone tree leucostoma caused by C. leucostoma, isolated mainly from the wood of live black cherry individuals, were visible, especially in plot III (Table A2). Species from the genus Cytospora are described as endophytes, saprotrophs, or phytopathogens. These pathogens cause cankers on the branches of various trees, such as peaches, nectarines, plums, ashes, maples, birches, and willows, and may lead to tree dieback [49]. The development of the pathogen is favored by stress factors, such as insect feeding or damage caused by hail, snow, or drought. Field observations (unpublished data) of leaves have indicated significant damage caused by the feeding of the monophagous moth Yponomeuta evonymellus L. (Lepidoptera) and polyphagous beetles, such as Gonioctena quinquepunctata F. and Phyllobius sp. (Coleoptera), which prefer Prunus padus L. and P. serotina leaves [50,51,52,53]. Wounds are the gateway to infection by pathogens of this type [54]. Both of the abovementioned fungus species can naturally support the methods used to reduce the occurrence of black cherry.
The presence of the following fungi in black cherry wood may positively limit its expansion: D. macrostoma (Phoma macrostoma), P. laundoniae, F. avenaceum, and Stemphylium sp. These are endophytes but can also transform from opportunists into pathogens after contact under appropriate conditions with a suitable host [55,56,57,58]. The fungi of the genus Stemphylium, which also infect plants of the genus Prunus [59], and Fusarium sp., whose presence in black cherry wood has also been confirmed [26], are interesting. On the research plots, numerous weakened P. serotina sprouts were observed with powdery mildew on their leaves (unpublished data), a symptom similar to those caused by Stemphylium pathogens. The natural presence of these species in black cherry wood is interesting, and their infectious potential could help limit the expansion and regrowth of P. serotina, especially since the lack of natural enemies is a major reason for the success of invasive species [60].
Dothiora prunorum (Aureobasidium prunorum) is a fungus classified as yeast, which was isolated from the fruit of Prunus domestica var. Belle de Louvain [61]. It has been recognized as an endophyte of crops [62]. Its role, similar to that of Epicoccum sp., is not clear. The genus Epicoccum includes endophytes, pathogens, saprotrophs, and antagonists to other pathogens [63]. These taxa should be further analyzed to determine their role in black cherry tissues. Further research should also be conducted on Aspergillus parvulus, which dominated dead wood in plot V (>50% proportion; Table A2) because its function in the dead wood fungal community has not been recognized so far [64].
Species of the genus Penicillium were previously isolated from stumps of P. serotina [26] and roots of black cherry [65]. The high frequency of Penicillium is due to its preferences and ecological specialization, abundant sporulation, and the nature of its spores and their effective dispersal [66]. The abovementioned researchers suggest that Penicillium spp. fungi participate in the decomposition of wood components due to their cosmopolitan nature combined with their cellulolytic properties. The scale of this process is probably limited, and their role as promoters of black cherry wood decomposition should not be overestimated [27].
According to Tokarska-Guzik et al. [4], black cherry is an established species in Poland, and two main reasons for its invasiveness are its ability to escape from natural enemies [67] and the lower pathogenicity of new enemies due to the lack of coevolution [68]. Our research indicates that some pathogens can weaken its population, such as B. cinerea, C. leucostoma, D. macrostoma, P. laundoniae, F. avenaceum, and Stemphylium sp. Additionally, the presence of B. cinerea in its tissues indicates a different research direction: the need to determine the genetic diversity of the population of this invasive plant species. The hitherto unsatisfactory effects of introducing P. serotina, manifested in the low quality of the wood material (with small dimensions, such as a shrub or a small tree), may result from inbreeding, a result of low genetic diversity in its population.

5. Conclusions

The differences between the fungal communities inhabiting the wood of dead and living trees were confirmed regarding taxon diversity and abundance. The results of the research conducted in a protected area indicate that black cherry wood can be naturally colonized by many pathogen species that can limit its expansion. Such pathogens include B. cinerea, C. leucostoma, D. macrostoma, P. laundoniae, F. avenaceum, and Stemphylium sp. A natural promoter of black cherry stump decomposition, the potential of which should be tested in further research, is S. rugosum, whose proportion in the dead wood communities was significant. C. leucostoma is an interesting species causing the leucostoma of stone fruit trees. The infection of black cherry by this pathogen indicates its establishment and gives us hope that naturally occurring antagonists can slow down the rate of black cherry expansion. In addition, we propose that identifying fungal communities based on molecular biology techniques should be supplemented by an inventory of macroscopic fungi and other symptoms for a more accurate recognition of the condition of examined trees and to facilitate inferences.

Author Contributions

Conceptualization, J.B.-B., A.Ł., M.B., R.K.; methodology, J.B.-B.; software, A.Ł., J.B.-B.; formal analysis, J.B.-B., A.Ł., M.B.; investigation, A.Ł., R.K., M.B., J.B.-B., W.K., D.K.; resources, A.Ł., A.P.; data curation, A.Ł., M.B., J.B.-B.; writing—original draft preparation, M.B.; writing—review and editing, A.Ł., R.K., J.B.-B.; visualization A.Ł., M.B.; supervision, W.K.; project administration, A.Ł.; funding acquisition, A.Ł., R.K., M.B., J.B.-B., A.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Forest Fund by National Forest Holding State Forests (Poland) as part of a research project entitled “Alternatywna metoda ograniczania czeremchy amerykańskiej w Wielkopolskim Parku Narodowym” (contract no. EZ.0290.1.20.2022) on the basis of the contract: T/2022/14.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Acknowledgments

The authors would like to thank Elżbieta Borowiak, for her valuable contribution to the administration of our project.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table A1. Taxation description of the selected forest divisions on the basis of the forest inventory (data current for end of 2013; access to data (30 November 2022): Data Bank of Forests, Poland). Data for forests in Poland is refreshed once every 10 years during detailed inventory.
Table A1. Taxation description of the selected forest divisions on the basis of the forest inventory (data current for end of 2013; access to data (30 November 2022): Data Bank of Forests, Poland). Data for forests in Poland is refreshed once every 10 years during detailed inventory.
Forest Division
(GPS Coordinates)
Research Plot (no.)Area (ha)Forest Habitat TypesForest LayerTree SpeciesShare of Species in Layer (%)Age (Year)Mean DBH (cm)Mean height (m)
46c
(16.831801;
52.301139)
1. and 2.3.96fresh broadleaved forestCanopyPinus sylvestris
Betula pendula
80
20
48
48
21
22
22
23
UnderstoryPrunus serotina
Fagus sylvatica
Quercus petraea
60
20
20
20
20
20
5
4
3
34b
(16.827777;
52.312627)
3.0.97fresh broadleaved forestCanopyPinus sylvestris
Betula pendula
90
10
51
51
22
23
22
22
UnderstoryPrunus serotina10035810
37g
(16.824575;
52.307312)
4.6.11fresh mixed coniferous forestCanopyPinus sylvestris100793024
UnderstoryBetula pendula
Quercus petraea
Prunus serotina
Fagus sylvatica
50
20
20
10
25
25
25
25
12
9
10
13
11
10
9
29h
(16.815404;
52.316147)
5.4.89fresh broadleaved forestCanopy (first layer)Pinus sylvestris
Quercus petraea
90
10
79
79
28
28
24
23
Canopy (second layer)Quercus petraea100601917
Understory (first layer)Prunus serotina10040911
Understory (second layer)Prunus serotina10020
Shrub layerPrunus serotina

Appendix B

Table A2. Frequency of individual taxa, the share of which was greater than 0.05%. L and D symbols with numbers indicate samples collected from live and dead trees from plots 1 to 5 (see Section 2).
Table A2. Frequency of individual taxa, the share of which was greater than 0.05%. L and D symbols with numbers indicate samples collected from live and dead trees from plots 1 to 5 (see Section 2).
TaxonLiveDead
L1L2L3L4L5D1D2D3D4D5
Alternaria infectoria E.G. Simmons2.414.280.825.220.14------------0.01
Alternaria tenuissima (Kunze) Wiltshire1.722.882.614.210.43------0.01------
Ascocoryne cylichnium (Tul.) Korf---0.240.02------0.06------24.870.02
Aspergillus parvulus G. Smith0.011.310.04---------------0.0150.60
Aureobasidium pullulans (de Bary & Löwenthal) G. Arnaud2.936.651.140.160.180.01---0.03------
Botrytis cinerea Pers.3.861.580.310.0811.23---------------
Chaetosphaeria sp. Tul. & C.Tul.---0.030.01---0.080.040.02---1.81---
Cladosporium sp. Link0.603.311.600.460.100.01---0.01------
Coniophora arida (Fr.) P. Karst.---------------4.88---0.01------
Coniophora sp. DC.---------------------1.16------
Cordana pauciseptata Preuss---------------50.43---0.01------
Cylindrobasidium evolvens (Fr.) Jülich------------------8.22---------
Cytospora leucostoma (Pers.) Sacc.9.232.074.5510.6323.010.010.025.60---0.03
Desmazierella acicola Lib.---0.9518.71---------------------
Diaporthe eres Nitschke------0.13---------1.810.06------
Didymella macrostoma (Mont.) Qian Chen & L. Cai3.341.773.233.250.31---------------
Diplodia sapinea (Fr.) Fuckel2.014.535.4612.311.250.02------------
Dothiora prunorum (C. Dennis & Buhagiar) Crous1.831.960.193.350.03---------------
Epicoccum sp. Link24.2820.8026.1833.803.34------0.02------
Exophiala sp. J.W.Carmich.---0.03---0.01---1.630.03---0.010.02
Fusarium avenaceum (Fr.) Sacc.1.641.631.765.590.10---------------
Ganoderma adspersum (Schulzer) Donk---------------------13.22------
Ganoderma applanatum (Pers.) Pat.---------------------15.88------
Mucor moelleri (Vuill.) Lendn.---0.08------1.62---------------
Mucor plumbeus Bonord.0.431.730.360.98------------------
Myxarium varium Hauerslev------------------------1.70---
Penicillium bialowiezense K.W. Zaleski0.976.071.891.430.560.01---0.03------
Penicillium brevicompactum Dierckx0.181.120.240.210.13---------------
Penicillium camemberti Thom0.071.642.160.560.51------0.04------
Penicillium canescens Sopp2.731.250.220.1532.79------0.01------
Penicillium lilacinoechinulatum S. Abe0.090.200.04---7.21------0.01------
Penicillium sp. Link0.562.010.910.240.390.060.020.040.010.04
Penicillium waksmanii K.W. Zaleski2.162.470.870.432.550.700.010.08---0.01
Peniophora cinerea (Pers.) Cooke---0.010.020.050.01------43.22------
Peniophora sp. Cooke---------------------1.05------
Pezicula cinnamomea (DC.) Sacc.0.040.210.270.050.060.940.112.603.232.38
Pezicula sporulosa Verkley0.010.210.130.020.011.120.300.430.030.08
Phialocephala piceae (T.N. Sieber & Grünig) Rossman0.041.020.650.090.0512.450.971.670.210.45
Phoma laundoniae Boerema & Gruyter0.270.601.440.271.23---------------
Pluteus cervinus (Schaeff.) P. Kumm.---------------2.21------------
Pluteus rangifer Justo, E.F. Malysheva & Bulyonk.---------------1.73------------
Pyrenochaeta sp. De Not.---0.050.013.36---0.01------------
Stemphylium sp. Wallr0.140.272.830.190.01---------------
Stereum rugosum Pers.0.021---0.11------12.3384.865.6265.3918.28
Strasseria geniculata (Berk. & Broome) Höhn.12.030.010.01---------------------
Trichoderma atroviride P.Karst.1.200.040.040.010.010.01---0.01---0.02
Trichoderma koningiopsis Samuels, C. Suárez & H.C. Evans12.663.1412.133.157.110.240.016.990.2014.63
Trichoderma reesei E.G. Simmons1.750.020.25---0.13---------------
Trichoderma sp. Pers.0.980.100.020.010.102.20---0.01---0.11
Umbelopsis isabellina (Oudem.) W. Gams0.030.160.381.470.020.02---0.010.016.55
Vararia sp. P. Karst.---------------1.89------------

References

  1. Binggeli, P. Misuse of terminology and anthropomorphic concepts in the description of introduced species. Bull. Br. Ecol. Soc. 1994, 25, 10–13. [Google Scholar]
  2. Pyšek, P. On the terminology used in plant invasion studies. In Plant Lnvasions—General Aspects and Special Problems; Pyšek, P., Prach, K., Rejmanek, M., Wade, M., Eds.; Academic Publishing: Amsterdam, The Netherlands, 1994; pp. 71–81. ISBN 9-05-103097-5. [Google Scholar]
  3. Pyšek, P.; Richardson, D.M.; Rejmánek, M.; Webster, G.L.; Williamson, M.; Kirschner, J. Alien plants in checklists and floras: Towards better communication between taxonomists and ecologists. Taxon 2004, 53, 131–143. [Google Scholar] [CrossRef]
  4. Tokarska-Guzik, B.; Dajdok, Z.; Urbisz, A.; Zając, M.; Urbisz, A.; Danielewicz, W. Identification and categorization of alien plant species as a basis for management. Acta Bot. Sil. 2011, 6, 23–53. [Google Scholar]
  5. Villamagna, A.M.; Murphy, B.R. Ecological and socio-economic impacts of invasive water hyacinth (Eichhornia crassipes): A review. Freshw. Biol. 2010, 55, 282–298. [Google Scholar] [CrossRef]
  6. Kumar Rai, P.; Singh, J.S. Invasive alien plant species: Their impact on environment, ecosystem services and human health. Ecol. Indic. 2020, 111, 106020. [Google Scholar] [CrossRef] [PubMed]
  7. Najberek, K.; Solarz, W.; Pusz, W.; Patejuk, K.; Olejniczak, P. Two sides of the same coin: Does alien Impatiens balfourii fall into an ecological trap after releasing from enemies? Environ. Exp. Bot. 2020, 176, 104103. [Google Scholar] [CrossRef]
  8. Kempel, A.; Nater, P.; Fischer, M.; van Kleunen, M. Plant-microbe-herbivore interactions in invasive and non-invasive alien plant species. Funct. Ecol. 2013, 27, 498–508. [Google Scholar] [CrossRef]
  9. Langmaier, M.; Lapin, K. A systematic review of the impact of invasive alien plants on forest regeneration in european temperate forests. Front. Plant Sci. 2020, 11, 1–15. [Google Scholar] [CrossRef]
  10. Rai, P.K.; Singh, J.S. Plant invasion in protected areas, the Indian Himalayan region, and the North East India: Progress and prospects. Proc. Indian Natl. Sci. Acad. 2021, 87, 19–35. [Google Scholar] [CrossRef]
  11. Foxcroft, L.C.; Pyšek, P.; Richardson, D.M.; Genovesi, P.; MacFadyen, S. Plant invasion science in protected areas: Progress and priorities. Biol. Invasions 2017, 19, 1353–1378. [Google Scholar] [CrossRef]
  12. Rejmánek, M.; Richardson, D.M. Trees and shrubs as invasive alien species—2013 update of the global database. Divers. Distrib. 2013, 19, 1093–1094. [Google Scholar] [CrossRef]
  13. Brunel, S.; Branquart, E.; Fried, G.; Van Valkenburg, J.; Brundu, G.; Starfinger, U.; Buholzer, S.; Uludag, A.; Joseffson, M.; Baker, R. The EPPO prioritization process for invasive alien plants. EPPO Bull. 2010, 40, 407–422. [Google Scholar] [CrossRef]
  14. Starfinger, U.; Kowarik, I.; Rode, M.; Schepker, H. From desirable ornamental plant to pest to accepted addition to the flora?—The perception of an alien tree species through the centuries. Biol. Invasions 2003, 5, 323–335. [Google Scholar] [CrossRef]
  15. Dyderski, M.K.; Jagodziński, A.M. Encroachment of Padus serotina (Ehrh.) Borkh.into alder carrs and ash-alder riparian forests. Acta Sci. Pol. Silv. Colendar. Rat. Ind. Lingar. 2015, 14, 103–113. [Google Scholar] [CrossRef]
  16. Najberek, K.; Solarz, W. Inwazje biologiczne w polskich parkach narodowych i krajobrazowych. In Gatunki Obce w Faunie Polski; Głowaciński, Z., Okarma, H., Pawłowski, J., Solarz, W., Eds.; Instytut Ochrony Przyrody Polskiej Akademii Nauk: Krakow, Poland, 2011; pp. 624–639. [Google Scholar]
  17. Namura-Ochalska, A. Walka z czeremchą amerykańską Padus serotina (Ehrh.) Borkh.—Ocena skuteczności wybranych metod w kampinoskim parku narodowym. Stud. I Mater. CEPL 2012, 33, 190–200. [Google Scholar]
  18. Namura-Ochalska, A.; Borowa, B. Walka z czeremchą amerykańską Padus serotina (Ehrh.) Borkh. w leśnictwie Rózin w Kampinoskim Parku Narodowym. In Zwalczanie Inwazyjnych Gatunków Roślin Obcego Pochodzenia—Dobre i Złe Doświadczenia; Krzysztofiak, L., Krzysztofiak, A., Eds.; Stowarzyszenie Człowiek i Przyroda: Krzywe, Poland, 2015; pp. 57–72. [Google Scholar]
  19. Tittenbrun, A.; Radliński, B. Praktyka zwalczania inwazyjnych gatunków obcych w Roztoczańskim Parku Narodowym. In Zwalczanie Inwazyjnych Gatunków Roślin Obcego Pochodzenia—Dobre i Złe Doświadczenia; Krzysztofiak, L., Krzysztofiak, A., Eds.; Stowarzyszenie Człowiek i Przyroda: Krzywe, Poland, 2015; pp. 49–54. [Google Scholar]
  20. Bien, S.; Damm, U. Prunus trees in Germany—A hideout of unknown fungi? Mycol. Prog. 2020, 19, 667–690. [Google Scholar] [CrossRef]
  21. Terwei, A. Prunus serotina (black cherry). CABI Compend. 2022. [Google Scholar] [CrossRef]
  22. Van den Meersschaut, D.; Lust, N. Comparison of mechanical, biological and chemical methods for controlling black cherry (Prunus serotina) in Flanders (Belgium). Silva Gandav. 1997, 62, 90–109. [Google Scholar] [CrossRef] [Green Version]
  23. De Jong, M.D. The BioChon story: Deployment of Chondrostereum purpureum to suppress stump sprouting in hardwoods. Mycologist 2000, 14, 58–62. [Google Scholar] [CrossRef]
  24. Roy, V.; Dubeau, D.; Auger, I. Biological control of intolerant hardwood competition: Silvicultural efficacy of Chondrostereum purpureum and worker productivity in conifer plantations. For. Ecol. Manag. 2010, 259, 1571–1579. [Google Scholar] [CrossRef]
  25. Fernando, W.G.D.; Zhang, J.X.; Chen, C.Q.; Remphrey, W.R.; Schurko, A.; Klassen, G.R. Molecular and morphological characteristics of Apiosporina morbosa, the causal agent of black knot in Prunus spp. Can. J. Plant Pathol. 2005, 27, 364–375. [Google Scholar] [CrossRef]
  26. Korzeniewicz, R.; Baranowska, M.; Behnke-Borowczyk, J. The effect of size of black cherry stumps on the composition of fungal communities colonising stumps. Open Life Sci. 2019, 14, 482–493. [Google Scholar] [CrossRef]
  27. Korzeniewicz, R.; Baranowska, M.; Kwaśna, H.; Niedbała, G.; Behnke-Borowczyk, J. Communities of fungi in black cherry stumps and effects of herbicide. Plants 2020, 9, 1126. [Google Scholar] [CrossRef] [PubMed]
  28. Baranowska, M.; Korzeniewicz, R.; Kartawik, N.; Behnke-Borowczyk, J. Seasonal changes in fungi colonies inhabiting black cherry stumps. Sylwan 2019, 163, 872–880. [Google Scholar]
  29. Marciszewska, K.; Szczepkowski, A.; Otręba, A.; Oktaba, L.; Kondras, M.; Zaniewski, P.; Ciurzycki, W.; Wojtan, R. The dynamics of sprouts generation and colonization by macrofungi of black cherry Prunus serotina Ehrh. eliminated mechanically in the Kampinos National Park. Folia For. Pol. Ser. A 2018, 60, 34–51. [Google Scholar] [CrossRef] [Green Version]
  30. Vilgalys, R.; Gonzalez, D. Organization of ribosomal DNA in the basidiomycete Thanatephorus praticola. Curr. Genet. 1990, 18, 277–280. [Google Scholar] [CrossRef]
  31. Schmidt, P.-A.; Bálint, M.; Greshake, B.; Bandow, C.; Römbke, J.; Schmitt, I. Illumina metabarcoding of a soil fungal community. Soil Biol. Biochem. 2013, 65, 128–132. [Google Scholar] [CrossRef]
  32. Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I.; et al. QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat. Publ. Gr. 2010, 7, 335–336. [Google Scholar] [CrossRef] [Green Version]
  33. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011, 17, 10. [Google Scholar] [CrossRef]
  34. Aronesty, E. Ea-Utils: “Command-Line Tools for Processing Biological Sequencing Data”. 2011. Available online: https://github.com/ExpressionAnalysis/ea-utils (accessed on 1 April 2023).
  35. Benson, D.A.; Cavanaugh, M.; Clark, K.; Karsch-Mizrachi, I.; Lipman, D.J.; Ostell, J.; Sayers, E.W. GenBank. Nucleic Acids Res. 2017, 45, D37–D42. [Google Scholar] [CrossRef] [Green Version]
  36. Põlme, S.; Abarenkov, K.; Henrik Nilsson, R.; Lindahl, B.D.; Clemmensen, K.E.; Kauserud, H.; Nguyen, N.; Kjøller, R.; Bates, S.T.; Baldrian, P.; et al. FungalTraits: A user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Divers. 2020, 105, 1–16. [Google Scholar] [CrossRef]
  37. R Development Core Team. R: A Language and Environment for Statistical Computing; R Fundation for Statistical Computing: Vienna, Austria, 2023; Available online: http://www.R-project.org (accessed on 1 April 2023).
  38. Bliss, C.I. The transformation of percentages for use in the analysis of variance. Ohio J. Sci. 1938, 38, 9–12. [Google Scholar]
  39. Anderson, M.J. Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef Stat. Ref. Online 2017, 1–15. [Google Scholar] [CrossRef]
  40. Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Sólymos, P.; Stevens, M.H.H.; Wagner, H. Vegan: Community Ecology Package Software. 2018. Available online: https://CRAN.R-project.org/package=vegan (accessed on 2 April 2023).
  41. Kwaśna, H.; Mazur, A.; Łabędzki, A.; Kuźmiński, R.; Łakomy, P. Communities of fungi in decomposed wood of oak and pine. For. Res. Pap. 2016, 77, 261–275. [Google Scholar] [CrossRef] [Green Version]
  42. Rayner, A.D.M.; Turton, M.N. Mycelial interactions and population structure in the genus Stereum: S. rugosum, S. sanguinolentum and S. rameale. Trans. Br. Mycol. Soc. 1982, 78, 483–493. [Google Scholar] [CrossRef]
  43. Tanney, J.B.; Douglas, B.; Seifert, K.A. Sexual and asexual states of some endophytic Phialocephala species of Picea. Mycologia 2016, 108, 255–280. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Kowalski, T.; Kehr, R.D. Two new species of Phialocephala occurring on Picea and Alnus. Can. J. Bot. 1995, 73, 26–32. [Google Scholar] [CrossRef]
  45. Müller, M.M.; Hantula, J.; Wingfield, M.; Drenkhan, R. Diplodia sapinea found on Scots pine in Finland. For. Pathol. 2019, 49, e12483. [Google Scholar] [CrossRef] [Green Version]
  46. Blumenstein, K.; Bußkamp, J.; Langer, G.J.; Langer, E.J.; Terhonen, E. The diplodia tip blight pathogen Sphaeropsis sapinea is the most common fungus in Scots pines’ mycobiome, irrespective of health status—A case study from Germany. J. Fungi 2021, 7, 607. [Google Scholar] [CrossRef]
  47. Williamson, B.; Tudzynski, B.; Tudzynski, P.; Van Kan, J.A.L. Botrytis cinerea: The cause of grey mould disease. Mol. Plant Pathol. 2007, 8, 561–580. [Google Scholar] [CrossRef] [PubMed]
  48. Van Kan, J.A.L.; Stassen, J.H.M.; Mosbach, A.; Van Der Lee, T.A.J.; Faino, L.; Farmer, A.D.; Papasotiriou, D.G.; Zhou, S.; Seidl, M.F.; Cottam, E.; et al. A gapless genome sequence of the fungus Botrytis cinerea. Mol. Plant Pathol. 2017, 18, 75–89. [Google Scholar] [CrossRef] [Green Version]
  49. Pan, M.; Zhu, H.; Tian, C.; Huang, M.; Fan, X. Assessment of Cytospora isolates from conifer cankers in China, with the descriptions of four new Cytospora species. Front. Plant Sci. 2021, 12, 636460. [Google Scholar] [CrossRef]
  50. Karolewski, P.; Jagodziński, A.M.; Giertych, M.J.; Łukowski, A.; Baraniak, E.; Oleksyn, J. Invasive Prunus serotina—A new host for Yponomeuta evonymellus (Lepidoptera: Yponomeutidae)? Eur. J. Entomol. 2014, 111, 227–236. [Google Scholar] [CrossRef] [Green Version]
  51. Karolewski, P.; Łukowski, A.; Adamczyk, D.; Żmuda, M.; Giertych, M.J.; Mąderek, E. Species composition of arthropods on six understory plant species growing in high and low light conditions. Dendrobiology 2020, 84, 58–80. [Google Scholar] [CrossRef]
  52. Mąderek, E.; Łukowski, A.; Giertych, M.J.; Karolewski, P. Influence of native and alien Prunus species and light conditions on performance of the leaf beetle Gonioctena quinquepunctata. Entomol. Exp. Appl. 2015, 155, 193–205. [Google Scholar] [CrossRef]
  53. Łukowski, A.; Giertych, M.J.; Walczak, U.; Baraniak, E.; Karolewski, P. Light conditions affect the performance of Yponomeuta evonymellus on its native host Prunus padus and the alien Prunus serotina. Bull. Entomol. Res. 2017, 107, 208–216. [Google Scholar] [CrossRef] [PubMed]
  54. Miller, S.T.; Otto, K.L.; Sterle, D.; Minas, I.S.; Stewart, J.E. Preventive fungicidal control of Cytospora leucostoma in peach orchards in Colorado. Plant Dis. 2019, 103, 1138–1147. [Google Scholar] [CrossRef]
  55. Aveskamp, M.M.; De Gruyter, J.; Crous, P.W. Biology and recent developments in the systematics of Phoma, a complex genus of major quarantine significance. Fungal Divers. 2008, 31, 1–18. [Google Scholar]
  56. Bennett, A.; Ponder, M.M.; Garcia-Diaz, J. Phoma infections: Classification, potential food sources, and their clinical impact. Microorganisms 2018, 6, 58. [Google Scholar] [CrossRef] [Green Version]
  57. Guo, D.; Yuan, C.; Zhai, Y.; An, H.; Shang, X.; An, D. Citrus endophytic Fusarium avenaceum Gds-1 for the control of citrus blue mold. Chin. J. Pestic. Sci. 2020, 22, 782–790. [Google Scholar] [CrossRef]
  58. Xu, Z.L.; Zheng, N.; Cao, S.M.; Li, S.T.; Mo, T.X.; Qin, Y.Y.; Li, J.; Yang, R.Y. Secondary metabolites from the endophytic fungus Stemphylium lycopersici and their antibacterial activities. Chem. Nat. Compd. 2020, 56, 1162–1165. [Google Scholar] [CrossRef]
  59. Spadoni, A.; Ippolito, A.; Sanzani, S.M. First report of Stemphylium eturmiunum causing postharvest rot of sweet cherry in Italy. Crop Prot. 2020, 132, 105112. [Google Scholar] [CrossRef]
  60. Halarewicz, A. The reasons underlying the invasion of forest communities by black cherry, Prunus serotina and its subsequent consequences. For. Res. Pap. 2011, 72, 267–272. [Google Scholar] [CrossRef] [Green Version]
  61. Dennis, C.; Buhagiar, R.W.M. Comparative study of Aureobasidium pullulans, A. prunorum sp.nov. and Trichosporon pullulans. Trans. Br. Mycol. Soc. 1973, 60, 567–575. [Google Scholar] [CrossRef]
  62. Kachalkin, A.V.; Glushakova, A.M.; Venzhik, A.S. Presence of clinically significant endophytic yeasts in agricultural crops: Monitoring and ecological safety assessment. IOP Conf. Ser. Earth Environ. Sci. 2021, 723, 042005. [Google Scholar] [CrossRef]
  63. Taguiam, J.D.; Evallo, E.; Balendres, M.A. Epicoccum species: Ubiquitous plant pathogens and effective biological control agents. Eur. J. Plant Pathol. 2021, 159, 713–725. [Google Scholar] [CrossRef]
  64. Nordberg, H.; Cantor, M.; Dusheyko, S.; Hua, S.; Poliakov, A.; Shabalov, I.; Smirnova, T.; Grigoriev, I.V.; Dubchak, I. The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res. 2014, 42, 26–31. [Google Scholar] [CrossRef]
  65. Kwaśna, H.; Bateman, G.L.; Ward, E. Determining species diversity of microfungal communities in forest tree roots by pure-culture isolation and DNA sequencing. Appl. Soil Ecol. 2008, 40, 44–56. [Google Scholar] [CrossRef] [Green Version]
  66. Poszytek, K. Mikrobiologiczna utylizacja celulozy. Postep. Mikrobiol. 2016, 55, 132–146. [Google Scholar]
  67. Reinhart, K.O.; Tytgat, T.; Van der Putten, W.H.; Clay, K. Virulence of soil-borne pathogens and invasion by Prunus serotina. New Phytol. 2010, 186, 484–495. [Google Scholar] [CrossRef]
  68. Richardson, D.M.; Pyšek, P. Plant invasions: Merging the concepts of species invasiveness and community invasibility. Prog. Phys. Geogr. 2006, 30, 409–431. [Google Scholar] [CrossRef] [Green Version]
Figure 1. Proportion (mean and SE) of taxa assigned to classes in fungal communities from live and dead black cherry stumps (considered together) (%).
Figure 1. Proportion (mean and SE) of taxa assigned to classes in fungal communities from live and dead black cherry stumps (considered together) (%).
Forests 14 01324 g001
Figure 2. The most numerous taxa in fungal communities from live (x and grey line) and dead black cherry stumps (black dots and black line; considered together) [%]. An asterisk indicates a statistically significant difference, with p < 0.05. The letters in parentheses indicate the trophic groups of fungi: S—saprotroph, P—pathogen, and O—other.
Figure 2. The most numerous taxa in fungal communities from live (x and grey line) and dead black cherry stumps (black dots and black line; considered together) [%]. An asterisk indicates a statistically significant difference, with p < 0.05. The letters in parentheses indicate the trophic groups of fungi: S—saprotroph, P—pathogen, and O—other.
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Figure 3. Proportion of identified taxa assigned to trophic groups in fungal communities from live and dead black cherry stumps (considered together) (%).
Figure 3. Proportion of identified taxa assigned to trophic groups in fungal communities from live and dead black cherry stumps (considered together) (%).
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Figure 4. Results of the NMDS statistical analysis. × live trees, ● dead trees.
Figure 4. Results of the NMDS statistical analysis. × live trees, ● dead trees.
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Figure 5. Boxplots for Shannon’s index (H) (upper graph) and Berger–Parker dominance index (d) (lower graph) for living and dead trees. The mean value is marked with the symbol × in the figures.
Figure 5. Boxplots for Shannon’s index (H) (upper graph) and Berger–Parker dominance index (d) (lower graph) for living and dead trees. The mean value is marked with the symbol × in the figures.
Forests 14 01324 g005
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Baranowska, M.; Korzeniewicz, R.; Behnke-Borowczyk, J.; Kowalkowski, W.; Krupiński, D.; Purcel, A.; Łukowski, A. Fungal Community Taxa Differ in Diversity and Number between Live and Dead Prunus serotina Ehrh. Wood in a Protected Forest within Its Secondary Range of Distribution. Forests 2023, 14, 1324. https://doi.org/10.3390/f14071324

AMA Style

Baranowska M, Korzeniewicz R, Behnke-Borowczyk J, Kowalkowski W, Krupiński D, Purcel A, Łukowski A. Fungal Community Taxa Differ in Diversity and Number between Live and Dead Prunus serotina Ehrh. Wood in a Protected Forest within Its Secondary Range of Distribution. Forests. 2023; 14(7):1324. https://doi.org/10.3390/f14071324

Chicago/Turabian Style

Baranowska, Marlena, Robert Korzeniewicz, Jolanta Behnke-Borowczyk, Wojciech Kowalkowski, Dariusz Krupiński, Andrzej Purcel, and Adrian Łukowski. 2023. "Fungal Community Taxa Differ in Diversity and Number between Live and Dead Prunus serotina Ehrh. Wood in a Protected Forest within Its Secondary Range of Distribution" Forests 14, no. 7: 1324. https://doi.org/10.3390/f14071324

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