https://orcid.org/0000-0001-9660-3137
Figures
Abstract
In Ethiopia, Pinus radiata and Pinus patula are extensively cultivated. Both plantations frequently serve as habitats for edible fungi, providing economic and ecological importance. Our study aims were: (i) to investigate how plantation age and tree species influence the variety of edible fungi and sporocarps production; (ii) to determine edaphic factors contributing to variations in sporocarps composition; and (iii) to establish a relationship between the most influencing edaphic factors and the production of valuable edible mushrooms for both plantation types. Sporocarps were collected weekly from permanent plots (100 m2) established in 5-, 14-, and 28-year-old stands of both species in 2020. From each plot, composite soil samples were also collected to determine explanatory edaphic variables for sporocarps production and composition. A total of 24 edible species, comprising 21 saprophytic and three ectomycorrhizal ones were identified. Agaricus campestroides, Morchella sp., Suillus luteus, Lepista sordida, and Tylopilus niger were found in both plantations. Sporocarp yields showed significant variation, with the highest mean production in 28-year-old stands of both Pinus stands. Differences in sporocarps variety were also observed between the two plantations, influenced by factors such as pH, nitrogen, phosphorus, potassium, and cation exchange capacity. Bovista dermoxantha, Coprinellus domesticus, and A. campestroides made contributions to the variety. The linear regression models indicated that the abundance of specific fungi was significantly predicted by organic matter. This insight into the nutrient requirements of various fungal species can inform for a better plantation management to produce both wood and non-wood forest products. Additionally, higher sporocarps production in older stands suggests that retaining patches of mature trees after the final cut can enhance fungal habitat, promoting diversity and yield. Thus, implementing this approach could provide supplementary income opportunities from mushroom sales and enhance the economic outputs of plantations, while mature trees could serve as a source of fungal inoculum for new plantations.
Citation: Dejene T, Merga B, Martín-Pinto P (2023) Green trees preservation: A sustainable source of valuable mushrooms for Ethiopian local communities. PLoS ONE 18(11): e0294633. https://doi.org/10.1371/journal.pone.0294633
Editor: Marcela Pagano, Universidade Federal de Minas Gerais, BRAZIL
Received: October 2, 2023; Accepted: November 5, 2023; Published: November 29, 2023
Copyright: © 2023 Dejene et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: Data are available as Supporting information file.
Funding: Spanish Agency for International Development and Cooperation *** B.M. Erasmus Mundus.
Competing interests: The authors have declared that no competing interests exist.
1. Introduction
Forest fungal communities contain a wide range of species that contribute significantly to the development, functioning, and stability of ecosystems [1,2]. In addition, fungi are part of the livelihood of people living in different parts of the world [3–5]. Fungi have long been collected as valuable non-timber forest products (NTFPs), generating a cash income for market traders, as well as being used for local subsistence in food and as a traditional medicine [3,6,7]. These practices help rural people to reduce their vulnerability to poverty and, in some regions, forest fungi also serve as a seasonal coping food during food shortage periods, mainly in the rainy season when grain is scarce [8]. However, in developing countries, activities related to forest management are focused on maximizing wood products rather than NTFPs, among which forest fungi are the most neglected NTFP resource [9–11].
In Ethiopia, the growing demand for forest products and agricultural land has resulted in widespread deforestation of natural forests [12,13]. To address this issue, fast-growing tree plantations have been established, mainly as community forests, which has led to a significant increase in the number of exotic tree species in recent decades [13–15]. These exotic plantations have the potential to produce high-value timber and NTFPs [16,17], including wild edible fungi [18,19]. Although studies have been conducted to assess the overall fungal diversity and sporocarp production in Ethiopian forest systems, there is still a lack of specific knowledge about the diversity, sporocarp production, and factors influencing the variety of valuable fungal species in short-rotation plantations [2,19].
Pinus radiata and Pinus patula are fast-growing, exotic, commercial timber-producing tree species. They are cultivated extensively in areas with mean annual rainfall levels of between 700 and 1500 mm, depending on the agroecology and elevation aspects [16,17]. Vast areas of Pinus tree plantations have been established, including state-owned forests, and are now the third largest plantation species after Eucalyptus and Cupressus in terms of overall plantation area in Ethiopia [13,20]. Due to their adaptability to a wide range of ecological conditions and rapid growth rate, Pinus species are highly desirable for sawn timber, poles, and posts [16]. In Ethiopia, the rotation period of Pinus species in general is between 30 and 40 years [21], with maximum timber production achieved when trees are 26–30 years old [22]. The management of Pinus plantations in Ethiopia is based on traditional silvicultural systems, with clear felling followed by replanting the preferred management technique [22,23]. Both the short-rotation period and clear-felling may have a direct impact on ecosystem properties and associated fungal communities that are sensitive to this type of management [24].
In plantation forest system, the variety of fungal species is closely linked to various biotic and abiotic factors, such as stand age [25,26], elevation [27,28], tree productivity [29,30], and soil environment [31,32]. Vegetation factors, such as stand age and site species composition, can affect fungal communities and their productivity directly through host–fungi specificity or indirectly through resource inputs, such as root exudates and litterfall [33,34]. Previous studies have shown that tree species identity is a key factor governing soil microbial communities, particularly mycorrhizal fungi [35,36]. Furthermore, forest stand age can affect fungal community structure and function through changes in the quantity and quality of litter [37].
In plantation forests dominated by a single tree species and characterized by a long rotation, such as temperate or boreal forests, the fungal community is expected to be highly dependent on the type of tree species [38]. In tropical forest systems, where plantations are characterized by a short rotation system and traditional silvicultural practices, such as clear felling and replanting, the impact of tree species and other biotic and abiotic factors on the fungal variety has rarely been studied, particularly in Ethiopian forest systems [39]. However, appropriate management of Ethiopian plantation forests is crucial to provide wood products while maintaining ecosystem integrity to provide a more conducive environment for fungi [39–41]. Therefore, it is important to identify mechanisms that regulate edible fungal communities and their production of sporocarps alongside the growth of stands. This information can be obtained by examining the distribution patterns of fungi and changes in their associations over time, particularly in plantations with short-rotation periods.
The overall aim of this study was to generate knowledge that could aid the management of plantation forests in Ethiopia to produce both wood and non-wood forest products, particularly edible wild mushrooms, based on a green tree retention approach. This practice involves leaving some living trees in harvested areas to retain ecosystem complexity by maintaining some of the structural diversity of the original forest even after harvesting. The retained trees provide habitat and support for mycorrhizal fungi, which are essential for the growth and fruiting of many edible mushrooms [42], such as chanterelles, porcini, and morels [43]. Hence, this approach can benefit both commercial and non-commercial harvesters of edible mushrooms and provide ecological benefits, which could increase the value of Ethiopian plantation forests.
We hypothesized that the production of edible sporocarps in short-rotation P. patula and P. radiata plantation forests in Ethiopia would be correlated with stand age in a specific manner, anticipating that like other plantations, species richness and sporocarp production would be highest in the oldest stands. We also anticipated that the variety of edible fungi would differ between the two plantation forests because the variety would be driven mainly by vegetation and site conditions, such as soil. Our specific objectives were: (i) to investigate how plantation age and tree species influence the variety of edible fungi and sporocarp production; (ii) to determine edaphic factors contributing to variations in sporocarp composition; and (iii) to establish a relationship between the most influencing edaphic factor and the production of valuable edible mushrooms for both plantation types.
2. Materials and methods
2.1. Study areas
The study was conducted in Menagesha Suba and Wondo Genet in the Oromia and Sidama Regional states of Ethiopia, respectively. Menagesha Suba forest is located 30 km from Addis Ababa in the central part of Ethiopia, while Wondo Genet is located 265 km from Addis Ababa in southern Ethiopia. The climate of the study areas is characterized by the Woyna Dega agro-climatic type. The rainfall pattern is bimodal, with low rainfall during spring and the main rainy season during the summer. Comprehensive geographical descriptions of the forests are provided in Table 1. The topography of the study areas is extremely dissected, with alternating ridges and valleys dominating the landscape and soils that are characterized by sandy loams. Soils at higher altitudes are shallow with a rocky substrate. At lower altitudes, where most of the plantations are located, the soil is deep but less gravelly at the Menagesha Suba site [44].
Both Menagesha Suba and Wondo Genet have officially protected areas. In Menagesha Suba, 9,248 ha are protected, of which original natural forests account for 2,500 ha and plantation forests of different species account for 1,000 ha. Plantations were established on areas that had already been deforested for cultivation and comprise both indigenous and exotic tree species, including Juniperus procera, Eucalyptus globulus, P. radiata, P. patula, and Cupressus lusitanica. By contrast, the original vegetation of the Wondo Genet was destroyed long ago because of logging and clearance for cultivation [16]. Consequently, large plantations of exotic tree species were established and there is currently approximately 100 ha of non-native forests of different tree species growing in the study area. The three predominantly planted species are C. lusitanica, Grevillea robusta, and P. patula [16,47].
2.2. Experimental design and sporocarp sampling
We selected two different Pinus plantations (P. radiata and P. patula) with 5-year-old, 14-year-old, and 28-year-old stands, hereafter referred to as ‘young’, ‘medium-aged’, and ‘old’ stands, respectively. Sporocarp data were collected using transect methods, as described in previous studies [18,48]. In each stand, three 2 × 50 m (100 m2) plots were established at least 200 m apart [49], i.e., nine plots in total, as described in [50,51]. Experimental plots were randomly laid out in each stand to avoid confounding spatial effects inherent to such a plot-based design [52,53], and all experimental plots were analyzed as independent samples [54].
Sporocarps were collected once a week during the main rainy season between July and August 2020 as described in [55,56]. Fresh weight measurements of sporocarps of each species were carried out in situ, and abundance data were obtained for each plot. Specimens were photographed in the field and their ecological characteristics were noted to assist and facilitate taxa identification processes. Sample fruit bodies of each species were taken to the laboratory and dried. These specimens were used for microscopic examination as part of the species identification process. Also, the fieldworks in the forests of Wondo Genet and Menagesha Suba were carried out with full authorization granted by Wondo Genet College of Forestry, and Oromia Forest and Wildlife Enterprise respectively.
2.3. Sporocarp identification
Taxonomic classification was conducted by examining tissues and spores with an Optika B-350PL microscope in the laboratory. Small samples of dried sporocarp specimens were rehydrated and mounted in 5% KOH for evaluation and identification. Morphological features of fruit bodies were examined using appropriate monographs, including [57–60], to determine the genus and species of the macrofungal specimens. Up-to-date fungal taxa names and authors’ names were obtained from the Mycobank database (http://mycobank.org). Ecological classification of each species was assigned based on fungal traits, as described in [61]. In addition, the edibility of the collected fruiting bodies was assessed following the criteria described in [62]. Taxa described in the literature as both non-edible and edible were classified as non-edible. Taxa described in the literature as having doubtful edibility were classified as non-edible. Only species classified as edible by a large majority of the literature consulted were classified as edible fungi.
2.4. Soil sampling and analysis
Soil samples were collected at a depth of 10 cm from all experimental plots. Soil samples were collected from five soil cores within each plot: the center and the four corners and then the selected soil physicochemical parameters were analyzed. The analysis was conducted by Water Works Design and Supervision Enterprises Laboratory Service Sub-process in the Soil Fertility Section at Addis Ababa, Ethiopia. Soil pH and electrical conductivity (EC) in a 1:2.5 (soil: liquid ratio) suspension and the supernatant of the same suspension were measured using a pH meter and an EC meter, respectively [63]. The wet digestion method [64] was used to determine soil carbon content, and total nitrogen was analyzed using Kjeldahl digestion [65], distillation, and titration as described by [66] by oxidizing the organic matter (OM) in concentrated sulfuric acid solution (0.1 N H2SO4). The available phosphorus of soils was determined using a standard procedure [67]. Soil parameters (i.e., EC, K, Ca, Mg, and cation exchange capacity (CEC)) were extracted using the diethylenetriaminepentaacetic acid extraction method [68], and all these soil characteristics were measured using an atomic absorption spectrophotometer. Comprehensive soil descriptions of each plot established in both types of plantation forest are provided in Table 2.
2.5. Statistical analysis
We used Linear Mixed Effects models (LME, p ≤ 0.05, package Nlme) to analyze the effects of stand age and Pinus species on the total fungal yield [69], where stand age was defined as a fixed variable and Pinus species was added to the model as a random variable. To determine specific significant differences, Tukey’s test was applied to the fixed variable.
Relationships between sporocarp variety and edaphic variables were visualized using non-metric multidimensional scaling (NMDS) based on an abundance species data matrix and scaled soil data. A permutation based nonparametric MANOVA (PerMANOVA) [70] using Euclidean distance was performed to analyze differences in sporocarp communities between stand types. Isolines were also plotted on the NMDS ordinations for OM using the ordisurf function. Correlations between NMDS axes scores with explanatory variables were assessed using the envfit function in R. To assess the influence of edaphic variables on the fungal community, we performed a Mantel test (Bray–Curtis distance) on the total species matrix and scaled environmental parameters. In addition, an analysis of similarity percentages (SIMPER) [71] was performed to identify edible fungi that were most responsible for the observed patterns, and was also used to determine the percentage contribution of macrofungal species to significant dissimilarities between the two forest types [72]. The SIMPER analysis was performed using the sim function of the Vegan package in R [73].
3. Results
3.1. Number of species and fresh biomass production
In total, 24 edible wild mushrooms were collected from plots established in young, medium-aged, and old stands in P. patula and P. radiata plantation forests. Mean annual sporocarp production of edible species differed significantly among the three stand age groups (F = 7.65; p = 0.006; Fig 1A), with the highest mean production levels recorded in old stands (707.18 kg ha–1). This value was significantly higher than that of the young stands (p-old_p-young = 0.0049) but was not significantly different to the yield obtained in medium aged stands (p-old_p-medium = 0.051). Furthermore, the mean production of fresh sporocarps in medium and young stands did not differ significantly (p = 0.460; Fig 1A).
Box plot data showing the maximum and minimum values. Note: The bar in the box is the standard deviation of the mean. Yields with the same letter are not significantly different (p > 0.05).
The total mean annual fresh weight production of sporocarps in P. patula stands was 383.84 kg ha–1 year–1 and 836.55 kg ha–1 year–1 in P. radiata plantations. However, total fresh sporocarp production did not differ significantly between the two plantation types (F = 1.58, p = 0.070; Fig 1B).
Among the 24 edible macrofungal species found in study, Saprotrophs were the dominant guild (21 species; 87.5%), whereas only three species were ectomycorrhizal fungi (Table 3). Economically important edible fungal species, such as Tylopilus niger, Suillus luteus, and Morchella africana, were collected (Table 3). The edible species collected according to stand age and stand species, the proportion of the total biomass that each fungal species represented, and their life strategy are presented in Table 3.
Stand age was significantly correlated with OM in P. patula (R = 0.98; p < 0.05; S1 Fig) and P. radiata (R = 0.89; p < 0.05; S2 Fig) plantations. In P. patula stands, OM was correlated with both T. niger (R = 0.92; p < 0.05) and total yield (R = 0.97; p < 0.05), whereas in P. radiata stands, OM was correlated with S. luteus yield (R = 0.8; p < 0.05).
3.2. Variety of edible mushrooms and edaphic variables
Stand age had a significant influence on the variety of edible sporocarps (F = 1.83, R2 = 0.1961, p < 0.046; Fig 2A). Explanatory edaphic variables, such as pH, potassium, CEC, and nitrogen, were significantly correlated with sporocarp variety according to stand age (Table 4). NMDS (stress = 0.0754) based on Bray–Curtis distance followed by perMANOVA analyses indicated that the sporocarp variety of P. patula and P. radiata plantations differed significantly (F = 7.27, R2 = 0.312, p = 0.001; Fig 2B). Edaphic variables such as pH, potassium, CEC, nitrogen, and phosphorus were significantly correlated with edible sporocarp variety based on plantation type (p < 0.05; Table 4).
Note: Arrows represent environmental variables that were most significantly (p < 0.05) related to ordination. Soil organic matter content displayed as isolines in B.
Edaphic variables with highly significant effects on sporocarp variety are shown in bold (p ≤ 0.01).
When we analyzed the contribution of individual edible species to the dissimilarity (%) between the different stand age groups of P. patula and P. radiata plantations, Bovista dermoxantha was the only edible fungal species that contributed to the dissimilarity between young and medium-aged P. patula stands. B. dermoxantha also made the biggest contribution to the dissimilarity between young and old P. patula stands, followed by T. niger and Leucoagaricus rubrotinctus (Table 5). In P. radiata plantations, Agaricus campestroides, Hygrophoropsis aurantiaca, and Schizophyllum commune made the biggest contribution to the dissimilarity in sporocarp variety between young and medium stands, while A. campestroides, Lycoperdon cf umbrinum, and S. commune made the biggest contribution to the dissimilarity in sporocarp variety between young and old stands. These analyses suggest that A. campestroides plays a significant role in young and medium-aged P. radiata stands, and B. dermoxantha plays a significant role in medium-aged P. patula stands.
We found that T. niger, B. dermoxantha, Agaricus subedulis, and Coprinellus domesticus were specific to P. patula stands, while Suillus luteus, Morchella africana, and Macrolepiota africana were found exclusively in P. radiata stands. However, A. campestroides, Calvatia subtomentosa, and Hygrophoropsis aurantiaca were found in both P. patula and P. radiata plantations (Table 3).
Linear regression models indicated that total sporocarp yields in P. patula and P. radiata forests and of specific valuable fungal species were significantly predicted by OM (p < 0.05; Fig 3). In both plantation types, the model fits the data well and OM explained 94% and 20% of the variation in total sporocarp production in P. patula and P. radiata stands, respectively. Similarly, OM explained 82% and 67% of the variation in T. niger and S. luteus sporocarp production, respectively. The sign of the coefficient was positive for both, which indicates that as OM increases, sporocarp production also increased. Thus, mean sporocarp production would increase for every one unit increase in OM in the studied plantations.
Note: Blue circles represent observed soil organic matter (OM) values, black lines indicate line fit plots, and shaded areas indicate 95% confidence intervals.
4. Discussion
The demand for mushrooms has been steadily increasing over the past decade [3]. This trend highlights the commercial value of forests, which can be enhanced through managed timber harvesting that could potentially enhance the habitat for the production of valuable edible mushrooms [74]. Although previous studies have reported the availability of wild fungi in Ethiopia, information about the type and potential yields of wild edible fungal species in exotic plantations is scarce. The aim of this study was to analyze how the age of short-rotation Pinus plantations affects the production of edible mushrooms. We collected a total of 24 edible fungal species. Most of these edible species (21) were saprotrophs. Some species were collected exclusively from P. patula (e.g., T. niger) or P. radiata (e.g., S. luteus) stands. This supports previous findings by [2] that some valuable fungal species are found exclusively in a particular forest system, indicating that different fungal species have unique ecological requirements for fructification or sporocarp production [75]. Thus, understanding the ecological preferences of various fungal species is essential for designing effective management strategies to promote their growth and conservation in different plantation systems.
As expected, mushroom yields were significantly influenced by stand age, which supports the findings of previous studies of fungal communities in Ethiopian forests [18,76]. Total sporocarp fresh weight yields were significantly higher in old stands than those in young stands, indicating that sporocarp yields increased as Pinus stands of both plantation types matured. This can be explained by changes in the physicochemical characteristics of the soil as the stands develops. For example, as a forest stand matures, the humus layer develops [77–80] and the forest soil increases its capacity to buffer temperature and moisture [78]. Such conditions could enhance fungal growth and fruiting, particularly of saprotrophic fungi [81], which dominated the fungal communities in our collections. In addition, increased humidity and OM accumulation along the age gradient of P. patula and P. radiata stands may lead to a more diverse spatial distribution, which could enhance fruiting, particularly in older stands [82,83]. Furthermore, stand age is one of the most important factors influencing fungal community variety in plantation forests [45,84]. An increase in the soil OM content over time enhances soil microbial activities, and the variety of microhabitats increases as the canopy closes, which in turn increases sporocarp production [85]. This notion is consistent with the findings of [83], who reported that well-developed stands with higher levels of canopy cover had greater levels of fungal diversity.
Stand age also significantly affected the most valuable edible species. Approximately 33% of the species collected from all plantations have economic significance and are marketable [3], including Agaricus sp., Morchella sp., Suillus sp., Lepista sp., and Tylopilus sp. [3]. Most of these species were found in middle-aged and old stands, which agrees with previous studies indicating that older stands harbor valuable species and have higher sporocarp yields than younger stands [39]. Previous reports have also recognized these edible fungal species as commercial NTFPs [86], which could potentially enhance the economic performance of forests [87] and encourage local communities to plant and manage more plantations in their surroundings. Furthermore, in some tropical countries, some of these fungal species are exported as forest products to generate income [53]. Despite the comparatively low total sporocarp yields obtained from the Pinus plantations assessed in this study [39], the sporocarp biomass obtained provides an insight into the potential production levels of the two plantation types, particularly of the marketable species. Thus, forest managers in Menagesha Suba and Wondo Genet should consider the balance between timber production and fungal conservation for environmental and production purposes. Consequently, maintaining Pinus trees as shelter instead of clear-cutting the plantation may be a more effective way of preserving and promoting the diversity and production of edible fungi. Thus, stand age had a significant impact on the total yield and on the yield of the most valuable species. Furthermore, stand age is one of the most important factors influencing fungal community variety in plantation forests [45,84]. Studies have shown that fungal diversity tends to increase with stand age, with older forests having a more diverse and complex fungal community compared with younger forests [39,88].
B. dermoxantha and A. campestroides may play important ecological roles in either young or old Pinus plantations. As saprophytes, B. dermoxantha and A. campestroides decompose dead plant matter, releasing nutrients that can be taken up by growing trees [89]. This process helps to build the nutrient-rich soils that trees need to grow. Saprotrophs play important roles in nutrient cycling and in the maintenance of healthy soils. As trees age and begin to decline, fungi help to break down dead plant material, releasing trapped nutrients back into the soil [90]. This cycle is important in maintaining the long-term health and sustainability of Pinus plantations.
In general, most of the collected edible macrofungal species made a large contribution to dissimilarities in the edible fungal community between young and old stands of Pinus. This suggestion is in line with findings that revealed that as forests age, the structure and variety of the vegetation changes, which can affect fungal community variety and diversity [91,92]. Furthermore, the tree species planted in the plantation can also influence fungal community variety [93].
Our analyses also revealed that soil conditions, referred to as edaphic variables, played a significant role in shaping the sporocarp variety in the studied stands [94,95]. This is because different fungal taxa are likely to respond to edaphic variables in different ways, depending on their characteristics [96,97], and, thus, in turn, the variety of fungal communities is directly correlated with soil parameters [98]. Among the edaphic variables, pH was significantly associated with the total sporocarp composition. We also observed that some edaphic variables were associated with the higher end of the pH isolines, indicating that nitrogen, phosphorus, potassium, and CEC are directly related to pH gradients [99]. This might be because soil pH is an important factor that governs the variety of sporocarps in forests because it affects the availability of other essential nutrients such as nitrogen, phosphorus, and potassium [6,100]. The solubility and availability of these nutrients are also influenced by soil pH values [101,102]. Thus, changes in pH can directly impact them, thus changing the variety of fungal communities in the forest ecosystem [103–105]. Nitrogen and phosphorus availability in the soil can also affect the distribution and abundance of fungal species in the forest [106]. Some fungi are better adapted to low-nitrogen environments and can thrive in nutrient-poor soils [107]. Potassium is another important nutrient for macrofungal species because it regulates osmotic pressure, maintains cell turgor, and balances cellular pH [108]. Thus, the availability of nitrogen, phosphorus, and potassium in the soil can influence the growth and development of fungal hyphae and affect the ability of macrofungi to compete with other microorganisms for soil resources [109,110]. Our study also revealed that the CEC is a contributing factor to sporocarp production. Although the specific role that CEC plays in sporocarp production is not yet fully understood, [111] noted that fungal species richness tends to be low when CEC is high. In our study, the majority of sporocarps collected in P. radiata stands were associated with low CEC values. This could be because soils with a high CEC are less likely to release base cations [112], which is an important factor in the distribution of macrofungal species. Base elements are crucial in many physicochemical processes, such as photosynthesis and, therefore, can impact plant photosynthesis and the amount of carbon available to fungi in the soil [113,114].
As anticipated, distinct communities of edible sporocarp species were found in P. patula and P. radiata plantations. Differences in community variety can be attributed to variations in environmental conditions between P. patula and P. radiata plantations, such as pH, nutrient availability, and moisture, which can impact the growth and survival of different fungal species. For instance, certain fungal species may thrive in acidic soils while others may prefer more alkaline conditions [115,116]. In our study, the heterogeneous soil environment, coupled with high levels of rainfall, could create microhabitats in which specific fungal species would be able to grow and survive in a particular plantation type [2]. For instance, we found that T. niger, B. dermoxantha, A. subedulis, and Coprinellus domesticus were specific to P. patula stands, while S. luteus, Morchella africana, and Macrolepiota africana were exclusive to P. radiata stands.
Three of the 24 edible fungal species collected in this study were ectomycorrhizal, (i.e., T. niger, L. sordida, and S. luteus), and could form mutualistic relationships with the host tree species. These mutualistic species are important for maintaining the health and productivity of plantation forests in our study areas. Agaricus campestroides, Calvatia subtomentosa, and Hygrophoropsis aurantiaca were common to both P. patula and P. radiata plantations, indicating that these genera might be characterized as generalists. Generalist fungal species are important for maintaining ecosystem functioning, biodiversity conservation, and can act as indicator species in forest ecosystems [117,118]. Thus, the presence of generalist fungal species can provide valuable information about the health and condition of forest ecosystems and indicate the role of plantation tree species in supporting a range of fungal species, which might be crucial for maintaining the overall functioning of forest ecosystems [43,119,120].
In addition, we found a correlation between OM and T. niger and S. luteus sporocarp production in P. patula and P. radiata plantations, respectively. This relationship could be attributed to the fact that mycorrhizal fungi tend to expand their mycelial network at the soil interface [121,122], where OM can influence the growth and network formation of mycelia [123]. Although a single growing season’s worth of data is insufficient to establish a clear relationship between soil OM and macrofungi, our preliminary findings suggest that soil OM content is directly associated with the overall richness and abundance of macrofungal species, a finding that is consistent with previous studies conducted by [39,124].
5. Conclusions
In this study, we investigated the influence of stand age on edible sporocarp production in Ethiopian short-rotation Pinus plantations. Stand age was shown to make a significant contribution to variations in fungal sporocarp production. Most of the collected species were found in old stands of P. patula and P. radiata, likely due to the greater availability of suitable substrates for fungal growth and sporocarp production in older stands than in younger stands. Therefore, preserving mature Pinus stands as shelter rather than clear-cutting them may be a more effective approach to promoting valuable fungal species and their sporocarp production. Moreover, edaphic variables were also found to be significantly correlated with sporocarp production in both P. patula and P. radiata plantations, suggesting that nutrient availability in the soil can influence edible fungal variety and sporocarp production. Thus, understanding the nutrient requirements of different fungal species can help us to better manage and conserve forest plantations to produce both timber and mushrooms as NTFPs. Hence, using a tree retention management approach in short-rotation Pinus plantations could be beneficial, leaving patches of live standing mature trees after the final rotation cut, which could increase habitat availability for saprophytic fungi owing to increased soil fertility, thereby increasing fungal diversity and edible sporocarp production. This method also provides live standing trees for mycorrhizal species such as T. niger and S. luteus after the final rotation cut, resulting in greater mycorrhizal sporocarp production. Some of the species collected in P. patula and P. radiata plantations also have potential economic value as the collections of edible mushrooms could create livelihoods in areas where economic alternatives may be limited. Moreover, the sale of mushrooms can generate revenue, and, hence, could provide additional income to forest managers and benefit especially small-scale collectors from the local communities. Furthermore, mushrooms also play a vital role in fostering sustainable forest management by enhancing soil health, nutrient cycling, and acting as indicators of ecosystem well-being. These contributions underscore the holistic significance of mushrooms in maintaining the vitality and economic sustainability of plantation forests. Thus, the approach of preserving mature Pinus stands could provide additional income opportunities for the rural population through the sale of mushrooms while promoting biodiversity conservation by balancing timber and fungal production.
Supporting information
S1 Fig. Scatter plot matrices showing Pearson correlation coefficients between edaphic variables and significance levels for total sporocarp production and edaphic parameters in the Pinus patula stands.
Abbreviations: EC, Electrical Conductivity; K, Potassium; Ca, Calcium; Mg, Magnesium; CEC, Cation Exchange Capacity; OM, Organic Matter; N, Nitrogen; P, Phosphors. On the bottom of the diagonal, bi-variate scatter plots with a fitted line are displayed. On the top of the diagonal, the value of the Pearson correlation is shown, plus the significance level of the p-values, which are indicated by asterisks. p-values: ***, < 0.001; **, < 0.01; and *, < 0.05.
https://doi.org/10.1371/journal.pone.0294633.s001
(TIF)
S2 Fig. Scatter plot matrices showing Pearson correlation coefficients between edaphic variables and significance levels for total sporocarp production and edaphic parameters in the Pinus radiata stands.
Abbreviations: EC, Electrical Conductivity; K, Potassium; Ca, Calcium; Mg, Magnesium; CEC, Cation Exchange Capacity; OM, Organic Matter; N, Nitrogen; P, Phosphors. On the bottom of the diagonal, bi-variate scatter plots with a fitted line are displayed. On the top of the diagonal, the value of the Pearson correlation is shown, plus the significance level of the p-values, which are indicated by asterisks. p-values: ***, < 0.001; **, < 0.01; and *, < 0.05.
https://doi.org/10.1371/journal.pone.0294633.s002
(TIF)
S1 File. Edible wild mushrooms and their total fresh biomass (kg ha-1year-1) collected in study plots in Pinus patula and Pinus radiata plantations located in Menagesha Suba and Wondo Genet, Ethiopia.
https://doi.org/10.1371/journal.pone.0294633.s003
(XLSX)
Acknowledgments
We would like to express our gratitude to the individuals who participated in the in the fieldwork in Wondo Genet and Menagesha Suba forest areas, Ethiopia. Furthermore, we acknowledge Dr. Caroline Woods for her language review and enhancement of the manuscript.
References
- 1. Vázquez-Veloso A, Dejene T, Oria-de-Rueda JA, Guijarro M, Hernando C, Espinosa J, et al. Prescribed burning in spring or autumn did not affect the soil fungal community in Mediterranean Pinus nigra natural forests. For Ecol Manage. 2022;512: 120161.
- 2. Kewessa G, Dejene T, Alem D, Tolera M, Martín-Pinto P. Forest Type and Site Conditions Influence the Diversity and Biomass of Edible Macrofungal Species in Ethiopia. J Fungi. 2022;8: 1023. pmid:36294588
- 3.
Boa E. Wild edible fungi: A global overview of their use and importance to people, Non-wood Forest Products. FAO, Rome. 2004;17.
- 4. Manoharachary C, Sridhar K, Singh R, Adholeya A, Suryanarayanan TS, Rawat S, et al. Fungal biodiversity: Distribution, conservation and prospecting of fungi from India. Current Science. 2005. pp. 58–71.
- 5. Sarma TC, Sarma I, Patiri BN. Edible mushroom used by some ethnic tribes of western Assam. The Bioscan. 2010;3: 613–625.
- 6.
Miles P., Chang ST. Mushrooms: cultivation, nutritional value, medicinal effect, and environmental impact. CRC press. 2004.
- 7.
Shackleton S, Delang CO, Angelsen A. From subsistence to safety nets and cash income: exploring the diverse values of non-timber forest products for livelihoods and poverty alleviation. Springer Berlin Heidelberg; 2011.
- 8. Fekadu A. Cultivation of Pleurotus ostreatus on Grevillea robusta leaves at Dilla University, Ethiopia. J Yeast Fungal Res. 2014;5: 74–83.
- 9. Asfaw Z, Tadesse M. Prospects for sustainable use and development of wild food plants in Ethiopia. Econ Bot. 2001;55: 47–62.
- 10. Lulekal E, Asfaw Z, Kelbessa E, Van Damme P. Wild edible plants in Ethiopia: a review on their potential to combat food insecurity. Afrika Focus. 2011;24: 71–122.
- 11. Melaku E, Ewnetu Z, Teketay D. Non-timber forest products and household incomes in Bonga forest area, southwestern Ethiopia. J For Res. 2014;25: 215–223.
- 12. Lemenih M, Kassa H. Re-greening Ethiopia: history, challenges and lessons. Forests. 2014;5: 1896–1909.
- 13. Tesfaye MA, Gardi O, Anbessa TB, Blaser J. Aboveground biomass, growth and yield for some selected introduced tree species, namely Cupressus lusitanica, Eucalyptus saligna, and Pinus patula in Central Highlands of Ethiopia. J Ecol Environ. 2020;44: 1–18.
- 14. Senbeta F, Teketay D. Regeneration of indigenous woody species under the canopies of tree plantations in Central Ethiopia. Trop Ecol. 2001;42: 175–185.
- 15.
Moges Y. The experiences of REDD+ for Ethiopian Condition. In Proceedings of the 1st technology dessimination workshop, 26th-27th November. 2015.
- 16. Teshome T. Analysis of resin and turpentine oil constituents of Pinus patula grown in Ethiopia. Ethiop e-Journal Res Innov foresight. 2011;3: 38–48.
- 17.
Thomas I, Bekele M. Role of planted forests and trees outside forests in sustainable forest management in the republic of Ethiopia. FAO. Rome; 2003. Report No.: FP/29E.
- 18. Dejene T, Oria-de-rueda JA, Martín-Pinto P. Fungal diversity and succession following stand development in Pinus patula Schiede ex Schltdl. & Cham. plantations in Ethiopia. For Ecol Manage. 2017;395: 9–18.
- 19. Alem D, Dejene T, Oria-de-Rueda JA, Martín-Pinto P. Survey of macrofungal diversity and analysis of edaphic factors influencing the fungal community of church forests in Dry Afromontane areas of Northern Ethiopia. For Ecol Manage. 2021;496: 119391.
- 20. Jaleta D, Mbilinyi B, Mahoo H, Lemenih M. Eucalyptus expansion as relieving and provocative tree in Ethiopia. J Agric Ecol Res Int. 2016;6: 1–12.
- 21. Tesfaye MA, Bravo-oviedo A, Bravo F, Kidane B, Bekele K, Sertse D, et al. Selection of Tree Species and Soil Management for Simultaneous Fuelwood Production and Soil Rehabilitation in the Ethiopian Central Highlands. L Degrad Dev. 2015;26: 665–679.
- 22.
Bekele M. Forest plantations and woodlots in Ethiopia. African For Forum. 2011. Report No.: 1.
- 23. Mekonnen Z, Kassa H, Lemenh M, Campbell B. The Role and Management of Eucalyptus in Lode Hetosa District, Central Ethiopia. For Trees Livelihoods. 2007;17: 309–323.
- 24. Paz CP, Gallon M, Putzke J, Ganade G. Changes in macrofungal communities following forest conversion into tree plantations in Southern Brazil. Biotropica. 2015;47: 616–625.
- 25. Zhu W, Cai X, Liu X, Wang J, Cheng S, Zhang X, et al. Soil microbial population dynamics along a chronosequence of moist evergreen broad-leaved forest succession in southwestern China. J Mt Sci. 2010;7: 327–338.
- 26. Wallander H, Johansson U, Sterkenburg E, Durling MB, Lindahl BD. Production of ectomycorrhizal mycelium peaks during canopy closure in Norway spruce forests. New Phytol. 2010;187: 1124–1134. pmid:20561206
- 27. Kernaghan G, Harper KA. Community structure of ectomycorrhizal fungi across an alpine/subalpine ecotone. Ecography (Cop). 2001;24: 181–188.
- 28. Bahram M, Põlme S, Kõljalg U, Zarre S, Tedersoo L. Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytol. 2012;193: 465–473. pmid:21988714
- 29. Kernaghan G. Mycorrhizal diversity: Cause and effect? Pedobiologia (Jena). 2005;49: 511–520.
- 30. Aučina A, Rudawska M, Leski T, Skridaila A, Riepšas E, Iwanski M. Growth and Mycorrhizal Community Structure of Pinus sylvestris Seedlings following the Addition of Forest Litter. Appl Environ Microbiol. 2007;73: 4867–4873. pmid:17575001
- 31. Peter M, Ayer F, Egli S. Nitrogen addition in a Norway spruce stand altered macromycete sporocarp production and below‐ground ectomycorrhizal species composition. New Phytol. 2001;149: 311–325. pmid:33874626
- 32. Dickie IA, Xu B, Koide RT. Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T‐RFLP analysis. New Phytol. 2002;156: 527–535. pmid:33873568
- 33. Alguacil MM, Torrecillas E, Lozano Z, Roldán A. Arbuscular mycorrhizal fungi communities in a coral cay system (Morrocoy, Venezuela) and their relationships with environmental variables. Sci Total Environ. 2015;505: 805–813. pmid:25461083
- 34. Billingsley Tobias T, Farrer EC, Rosales A, Sinsabaugh RL, Suding KN, Porras-Alfaro A. Seed-associated fungi in the alpine tundra: Both mutualists and pathogens could impact plant recruitment. Fungal Ecol. 2017;30: 10–18.
- 35. DeBellis T, Widden P. Diversity of the small subunit ribosomal RNA gene of the arbuscular mycorrhizal fungi colonizing Clintonia borealis from a mixed-wood boreal forest. FEMS Microbiol Ecol. 2006;58: 225–235. pmid:17064264
- 36. Horn S, Hempel S, Verbruggen E, Rillig MC, Caruso T. Linking the community structure of arbuscular mycorrhizal fungi and plants: A story of interdependence? ISME J. 2017;11: 1400–1411. pmid:28244977
- 37. Schilling EM, Waring BG, Schilling JS, Powers JS. Forest composition modifies litter dynamics and decomposition in regenerating tropical dry forest. Oecologia. 2016;182: 287–297. pmid:27236291
- 38. Wu YT, Wubet T, Trogisch S, Both S, Scholten T, Bruelheide H, et al. Forest age and plant species composition determine the soil fungal community composition in a Chinese subtropical forest. PLoS One. 2013;8: 1–12. pmid:23826151
- 39. Dejene T, Worku E, Martín-Pinto P. Retention of Matured Trees to Conserve Fungal Diversity and Edible Sporocarps from Short-Rotation Pinus radiata Plantations in Ethiopia. Plant Ethiop J Fungi. 2021;7: 702. pmid:34575740
- 40. Lindenmayer DB, Franklin JF, Lõhmus A, Baker SC, Bauhus J, Beese W, et al. A major shift to the retention approach for forestry can help resolve some global forest sustainability issues. Conserv Lett. 2012;5: 421–431.
- 41.
Nyland RD. Silviculture: concepts and applications. Waveland Press. 2016.
- 42. Luoma DL, Eberhart JL, Molina R, Amaranthus MP. Response of ectomycorrhizal fungus sporocarp production to varying levels and patterns of green-tree retention. For Ecol Manage. 2004;202: 337–354.
- 43. Pérez‐Moreno J, Guerin‐Laguette A, Rinaldi AC, Yu F, Verbeken A, Hernández‐Santiago F, et al. Edible mycorrhizal fungi of the world: What is their role in forest sustainability, food security, biocultural conservation and climate change? PLANTS, PEOPLE, PLANET. 2021;3: 471–490.
- 44. Bekele T. Vegetation ecology of remnant Afromontane forests on the Central Plateau of Shewa, Ethiopia. Acta Phytogeogr Suec. 1993;59: 1–59.
- 45. Alem D, Dejene T, Oria-de-Rueda JA, Geml J, Martín-Pinto P. Soil Fungal Communities under Pinus patula Schiede ex Schltdl. & Cham. Plantation Forests of Different Ages in Ethiopia. Forests. 2020;11: 1109.
- 46. Jemal A, Getu E. Diversity of butterfly communities at different altitudes of Menagesha-suba state forest, Ethiopia. J Entomol Zool Stud. 2018;6: 2197–2202.
- 47. Bekele T, Kassa K, Mengistu T, Debele M, Melka Y. Working with communities to address deforestation in the Wondo Genet catchment Area, Ethiopia: lessons learnt from a participatory action research. Res J Agric Environ Manag. 2013;2: 448–456.
- 48. Dejene T, Oria-de-Rueda JA, Martín-Pinto P. Fungal diversity and succession under Eucalyptus grandis plantations in Ethiopia. For Ecol Manage. 2017;405: 179–187.
- 49. Luoma DL, Frenkel RE, Trappe JM. Fruiting of hypogeous fungi in Oregon Douglas-Fir forests: seasonal and habitat variation. Mycologia. 1991;83: 335–353.
- 50. Gassibe PV, Fabero RF, Hernández-Rodríguez M, Oria-de-Rueda JA, Martín-Pinto P. Fungal community succession following wildfire in a Mediterranean vegetation type dominated by Pinus pinaster in Northwest Spain. For Ecol Manage. 2011;262: 655–662.
- 51. Hernández-Rodríguez M, Oria-de-Rueda JA, Pando V, Martín-Pinto P. Impact of fuel reduction treatments on fungal sporocarp production and diversity associated with Cistus ladanifer L. ecosystems. For Ecol Manage. 2015;353: 10–20.
- 52. Hiiesalu I, Bahram M, Tedersoo L. Plant species richness and productivity determine the diversity of soil fungal guilds in temperate coniferous forest and bog habitats. Mol Ecol. 2017;26: 4846–4858. pmid:28734072
- 53. Rudolph S, Schleuning M, Piepenbring M. Temporal variation of fungal diversity in a mosaic landscape in Germany. Stud Mycol. 2018. pmid:29910516
- 54. Ruiz-Almenara C, Gándara E, Gómez-Hernández M. Comparison of diversity and composition of macrofungal species between intensive mushroom harvesting and non-harvesting areas in Oaxaca, Mexico. PeerJ. 2019;7: e8325. pmid:31976170
- 55. Vásquez-Gassibe P, Oria-de-Rueda JA, Santos-del-Blanco L, Martín-Pinto P. The effects of fire severity on ectomycorrhizal colonization and morphometric features in Pinus pinaster Ait. seedlings. For Syst. 2016;25.
- 56. Hernández-Rodríguez M, Martín-Pinto P, Oria-de-Rueda JA, Diaz-Balteiro L. Optimal management of Cistus ladanifer shrublands for biomass and Boletus edulis mushroom production. Agrofor Syst. 2017;91: 663–676.
- 57. Antonin V. Monograph of Marasmius, Gloiocephala, Palaeocephala and Setulipes in Tropical Africa. Fungus Fl Trop Afr. 2007;1: 177.
- 58. Hama O, Maes E, Guissou M, Ibrahim D, Barrage M, Parra L, et al. Agaricus subsaharianus, une nouvelle espèce comestible et consomméeau Niger, au Burkina Faso et en Tanzanie. Crypto Mycol. 2010;31: 221–234.
- 59. Pegler DN. Studies on African Agaricales: II *. Kew Bull. 1969;23: 219–249.
- 60. Hjortstam K, Ryvarden L. New and interesting wood-inhabiting fungi (Basidiomycotina—Aphyllophorales) from Ethiopia. Mycotaxon. 1996;60: 181–190.
- 61. Põlme S, Abarenkov K, Henrik Nilsson R, Lindahl BD, Clemmensen KE, Kauserud H, et al. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Divers. 2020;105.
- 62. Bonet JA, Fischer CR, Colinas C. The relationship between forest age and aspect on the production of sporocarps of ectomycorrhizal fungi in Pinus sylvestris forests of the central Pyrenees. For Ecol Manage. 2004;203: 157–175.
- 63.
Van Reeuwijk LP. Procedures for Soil Analysis, International Soil Reference and Information Centre (ISRIC): Wageningen. 2002.
- 64. Walkley A, Black IA. An examination of the digestion method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci. 1934;34: 29–38.
- 65.
Tan KH. Soil sampling, preparation and analysis. Marcel Dekker, New York; 1996. pp. 139–145.
- 66. Black CA, Evans DD, Dinauer RC. Methods of soil analysis. Madison, WI Am Soc Agron. 1965;9: 653–708.
- 67.
Olsen SR. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture. 1954. p. No. 939.
- 68. Lindsay WL, Norvell WA. Development of a DTPA Soil Test for Zinc, Iron, Manganese, and Copper. Soil Sci Soc Am J. 1978;42: 421–428.
- 69.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., Team RC. Nlme: Linear and Nonlinear Mixed Effects Models. R Packag Version 31. 2016;128.
- 70. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26: 32–46.
- 71. Clarke KR. Non-parametric multivariate analyses of changes in community structure. Austral Ecol. 1993;18: 117–143.
- 72. Parravicini V, Micheli F, Montefalcone M, Villa E, Morri C, Bianchi CN. Rapid assessment of epibenthic communities: A comparison between two visual sampling techniques. J Exp Mar Bio Ecol. 2010;395: 21–29.
- 73.
R Core Team. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2020.
- 74. Bonet JA, Fischer CR, Colinas C. The relationship between forest age and aspect on the production of sporocarps of ectomycorrhizal fungi in Pinus sylvestris forests of the central Pyrenees. For Ecol Manage. 2004;203: 157–175.
- 75. Buée M, Courty PE, Mignot D, Garbaye J. Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biol Biochem. 2007;39: 1947–1955.
- 76. Dejene Agamy, Agúndez Martín-Pinto. Ethnobotanical Survey of Wild Edible Fruit Tree Species in Lowland Areas of Ethiopia. Forests. 2020;11: 177.
- 77. Dove N, Keeton W. Structural complexity enhancement increases fungal species richness in northern hardwood forests. Fungal Ecol. 2015;13: 181–192.
- 78. Pinna S, Gévry MF, Côté M, Sirois L. Factors influencing fructification phenology of edible mushrooms in a boreal mixed forest of Eastern Canada. For Ecol Manage. 2010;260: 294–301.
- 79. Toivanen T, Markkanen A, Kotiaho JS, Halme P. The effect of forest fuel harvesting on the fungal diversity of clear-cuts. Biomass and Bioenergy. 2012;39: 84–93.
- 80. Solly EF, Weber V, Zimmermann S, Walthert L, Hagedorn F, Schmidt MWI. A Critical Evaluation of the Relationship Between the Effective Cation Exchange Capacity and Soil Organic Carbon Content in Swiss Forest Soils. Front For Glob Chang. 2020;3: 1–12.
- 81. Fernández-Toirán LM, Ágreda T, Olano JM. Stand age and sampling year effect on the fungal fruit body community in Pinus pinaster forests in central Spain. Can J Bot. 2006;84: 1249–1258.
- 82. Köhl M, Lasco R, Cifuentes M, Jonsson Ö, Korhonen KT, Mundhenk P, et al. Changes in forest production, biomass and carbon: Results from the 2015 UN FAO Global Forest Resource Assessment. For Ecol Manage. 2015;352: 21–34.
- 83. Sysouphanthong P, Thongkantha S, Zhao R, Soytong K, Hyde KD. Mushroom diversity in sustainable shade tea forest and the effect of fire damage. Biodivers Conserv. 2010;19: 1401–1415.
- 84. Dang P, Yu X, Le H, Liu J, Shen Z, Zhao Z. Effects of stand age and soil properties on soil bacterial and fungal community composition in Chinese pine plantations on the Loess Plateau. Kothe E, editor. PLoS One. 2017;12: e0186501. pmid:29049349
- 85. Dove NC, Keeton WS. Structural complexity enhancement increases fungal species richness in northern hardwood forests. Fungal Ecol. 2015;13: 181–192.
- 86. Mortimer PE, Karunarathna SC, Li Q, Gui H, Yang X, Yang X, et al. Prized edible Asian mushrooms: Ecology, conservation and sustainability. Fungal Divers. 2012;56: 31–47.
- 87. Chapela IH, Osher LJ, Horton TR, Henn MR. Ectomycorrhizal fungi introduced with exotic pine plantations induce soil carbon depletion. Soil Biol Biochem. 2001;33: 1733–1740.
- 88. Twieg BD, Durall DM, Simard SW. Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol. 2007;176: 437–447. pmid:17888121
- 89. Owen SM, Patterson AM, Gehring CA, Sieg CH, Baggett LS, Fulé PZ. Large, high-severity burn patches limit fungal recovery 13 years after wildfire in a ponderosa pine forest. Soil Biol Biochem. 2019;139: 107616.
- 90.
Dighton J. Fungi in ecosystem processes, vol 17. New York, NY: Marcel Dekker; 2003.
- 91. Goldmann K, Schöning I, Buscot F, Wubet T. Forest Management Type Influences Diversity and Community Composition of Soil Fungi across Temperate Forest Ecosystems. Front Microbiol. 2015;6. pmid:26635766
- 92. Liu G, Chen L, Shi X, Yuan Z, Yuan LY, Lock TR, et al. Changes in rhizosphere bacterial and fungal community composition with vegetation restoration in planted forests. L Degrad Dev. 2019;30: 1147–1157.
- 93. Cao Y, Fu S, Zou X, Cao H, Shao Y, Zhou L. Soil microbial community composition under Eucalyptus plantations of different age in subtropical China. Eur J Soil Biol. 2010;46: 128–135.
- 94. Liang Y, He X, Chen C, Feng S, Liu L, Chen X, et al. Influence of plant communities and soil properties during natural vegetation restoration on arbuscular mycorrhizal fungal communities in a karst region. Ecol Eng. 2015;82: 57–65.
- 95. Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A. Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol. 2015;205: 1385–1388. pmid:25231111
- 96. Crowther TW, Stanton DWG, Thomas SM, A’Bear AD, Hiscox J, Jones TH, et al. Top-down control of soil fungal community composition by a globally distributed keystone consumer. Ecology. 2013;94: 2518–2528. pmid:24400503
- 97. Koide RT, Fernandez C, Malcolm G. Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function. New Phytol. 2014;201: 433–439. pmid:26207269
- 98. Cozzolino V, Di Meo V, Monda H, Spaccini R, Piccolo A. The molecular characteristics of compost affect plant growth, arbuscular mycorrhizal fungi, and soil microbial community composition. Biol Fertil Soils. 2016;52: 15–29.
- 99. Puangsombat P, Sangwanit U, Marod D. Diversity of soil fungi in different land use types in Tha Kum-Huai Raeng forest reserve, Trat Province. Kasetsart J (Nat Sci). 2010;44: 1162–1175.
- 100. Miransari M. Soil microbes and the availability of soil nutrients. Acta Physiol Plant. 2013;35: 3075–3084.
- 101. Sheng XF, He LY, Huang WY. The conditions of releasing potassium by a silicate-dissolving bacterial strain NBT. Agric Sci China. 2002;1: 662–666.
- 102. Sattar A, Naveed M, Ali M, Zahir ZA, Nadeem SM, Yaseen M, et al. Perspectives of potassium solubilizing microbes in sustainable food production system: A review. Appl Soil Ecol. 2019;133: 146–159.
- 103.
Finlay RD. Interactions between Soil Acidification, Plant Growth and Nutrient Uptake in Ectomycorrhizal Associations of Forest Trees Author (s): R. D. Finlay Source: Ecological Bulletins, 1995, No. 44, Effects of Acid Deposition and Tropospheric Ozone on F. 1995; 197–214.
- 104. Goldmann K, Schröter K, Pena R, Schöning I, Schrumpf M, Buscot F, et al. Divergent habitat filtering of root and soil fungal communities in temperate beech forests. Sci Rep. 2016;6: 1–10. pmid:27511465
- 105. Tauro TP, Mtambanengwe F, Mpepereki S, Mapfumo P. Soil fungal community structure and seasonal diversity following application of organic amendments of different quality under maize cropping in Zimbabwe. PLoS One. 2021;16: 1–20. pmid:34648549
- 106. Wallander H, Nylund J-E ‐E. Effects of excess nitrogen and phosphorus starvation on the extramatrical mycelium of ectomycorrhizas of Pinus sylvestris L. New Phytol. 1992;120: 495–503.
- 107. Lundeberg G. Utilisation of various nitrogen sources, in particular bound soil nitrogen, by mycorrhizal fungi. Stud For Suec. 1970;79: 1–95.
- 108.
Fazenda ML, Seviour R, McNeil B, Harvey LM. Submerged Culture Fermentation of “Higher Fungi”: The Macrofungi. 2008. pp. 33–103.
- 109. Dighton J. Acquisition of nutrients from organic resources by mycorrhizal autotrophic plants. Experientia. 1991;47: 362–369.
- 110.
Dighton J, Sridhar KR, Deshmukh SK. The Roles of Macro Fungi (Basidomycotina) in Terrestrial Ecosystems. Advances in Macrofungi: Diversity, Ecology and Biotechnology. CRC-Press, Boca Raton, USA. 2019. pp. 70–104.
- 111. Crabtree CD, Keller HW, Ely JS. Macrofungi associated with vegetation and soils at Ha Ha Tonka State Park, Missouri. Mycologia. 2010;102: 1229–1239. pmid:20943573
- 112. Zheng Q, Hu Y, Zhang S, Noll L, Böckle T, Dietrich M, et al. Soil multifunctionality is affected by the soil environment and by microbial community composition and diversity. Soil Biol Biochem. 2019;136: 107521. pmid:31700196
- 113. Shi L-L, Mortimer PE, Ferry Slik JW, Zou X-M, Xu J, Feng W-T, et al. Variation in forest soil fungal diversity along a latitudinal gradient. Fungal Divers. 2014;64: 305–315.
- 114. He D, Xiang X, He J-S, Wang C, Cao G, Adams J, et al. Composition of the soil fungal community is more sensitive to phosphorus than nitrogen addition in the alpine meadow on the Qinghai-Tibetan Plateau. Biol Fertil Soils. 2016;52: 1059–1072.
- 115. Rochon C, Paré D, Pélardy N, Khasa DP, Fortin JA. Ecology and productivity of Cantharellus cibarius var. roseocanus in two eastern Canadian jack pine stands. Botany. 2011;89: 663–675.
- 116. Hussain S, Sher H. Ecological characterization of Morel (Morchella spp.) habitats: A multivariate comparison from three forest types of district Swat, Pakistan. Acta Ecol Sin. 2021;41: 1–9.
- 117. Brockerhoff EG, Barbaro L, Castagneyrol B, Forrester DI, Gardiner B, González-Olabarria JR, et al. Forest biodiversity, ecosystem functioning and the provision of ecosystem services. Biodivers Conserv. 2017;26: 3005–3035.
- 118.
Wubet T, Christ S, Schö Ning I, Boch S, Gawlich M, Schnabel B, et al. Differences in Soil Fungal Communities between European Beech (Fagus sylvatica L.) Dominated Forests Are Related to Soil and Understory Vegetation. 2012.
- 119. Brundrett M. Diversity and classification of mycorrhizal associations. Biol Rev. 2004;79: 473–495. pmid:15366760
- 120. Allen EB, Allem MF, Helm DJ, Trappe JM, Molina R, Rincon E. Patterns and regulation of arbuscular and ectomycrrhizal plant and fungal diversity: a hypothesis. Plant Soil. 1992;170: 47–62.
- 121. Boddy L, Hynes J, Bebber DP, Fricker MD. Saprotrophic cord systems: Dispersal mechanisms in space and time. Mycoscience. 2009;50: 9–19.
- 122. Sommermann L, Geistlinger J, Wibberg D, Deubel A, Zwanzig J, Babin D, et al. Fungal community profiles in agricultural soils of a long-term field trial under different tillage, fertilization and crop rotation conditions analyzed by high-throughput ITS-amplicon sequencing. PLoS ONE. 2018. pmid:29621291
- 123. Zakaria AJ, Boddy L. Mycelial foraging by Resinicium bicolor: Interactive effects of resource quantity, quality and soil composition. FEMS Microbiol Ecol. 2002;40: 135–142. pmid:19709220
- 124. Eaton RJ, Barbercheck M, Buford M, Smith W. Effects of organic matter removal, soil compaction, and vegetation control on Collembolan populations. Pedobiologia (Jena). 2004;48: 121–128.