1-S2.0-S0378112722004455-Main HONGOS EUROPA
1-S2.0-S0378112722004455-Main HONGOS EUROPA
A R T I C L E I N F O A B S T R A C T
Keywords: Mushrooms play an important role in the maintenance of ecosystem processes and delivering ecosystem services,
Diversity-productivity interaction including food supply. They are also an important source of income for many people worldwide. Thus, under
Forest goods standing which environmental factors influence mushroom productivity is a high practical and scientific priority.
Ecosystem services
We monitored the production of mushrooms in temperate mixed deciduous forest in Białowieża Primeval Forest
Dr. FOREST
BiodivERsA
in eastern Poland for two yielding seasons. The research plots were set under similar environmental conditions
FundivEUROPE (topography, geology, soil type) but differed by tree species composition and tree species richness. The main
factor explaining mushroom production (close to 35% of the variation explained by the model) was the species
richness of mushrooms. In turn, the species richness of mushrooms was mainly explained by soil properties (pH
and C/N ratio) and stand characteristics (including tree species richness and wood increment) for ectomycor
rhizal mushrooms and by soil pH for saprotrophic mushrooms. Higher precipitation in 2021 resulted in higher
mushroom production than in 2020, while low levels of precipitation in 2020 resulted in stronger effect of
ambient temperature. The differences in mushroom yield between years varied highly among plots. They were
explained by stand characteristics, and in the case of saprotrophic mushrooms by tree richness and their own
species richness. Our results suggest that promoting mushroom species richness is fundamental for increasing
mushroom yield and should be taken into account in forest management.
* Corresponding author.
E-mail address: [email protected] (B. Jaroszewicz).
https://doi.org/10.1016/j.foreco.2022.120451
Received 10 June 2022; Received in revised form 29 July 2022; Accepted 31 July 2022
Available online 11 August 2022
0378-1127/© 2022 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
K. Stojek et al. Forest Ecology and Management 522 (2022) 120451
environment – mostly forests (Savoie and Largeteau, 2011). Therefore, this point of view depends on tree species composition and soil prop
examining the environmental factors affecting mushroom production is erties (de-Miguel et al., 2014).
a key element in enhancing the availability of mushrooms as an Despite many studies researching factors affecting mushroom pro
important element of the human diet and wellbeing. duction, knowledge on the impact of tree species composition on
The main factors affecting the production of forest mushrooms are mushroom yield is scarce. Tree identity and tree species richness influ
weather conditions, access to nutrient sources, forest management, and ence the fungal biomass and species composition of fungi. Urbanová
forest stand characteristics. Ambient temperature, soil humidity, and et al. (2015) reported that in mixed temperate forests fungal taxa are
especially precipitation in the summer and autumn seem to be the most often tree specific: 35–37 % of the dominant fungal operational taxo
important factors explaining differences in mushroom production be nomic units (OTUs) were restricted only to one or two trees. In this
tween years (Karavani et al., 2018; Alday et al., 2017a; Taye et al., study, numbers of observed dominant OTUs increased with the
2016). In a 21-year long survey carried out in Switzerland, a noticeable increasing number of trees, suggesting the great role of tree species
variation in the production and species richness of mushrooms between richness in forming fungal communities. They also revealed that tree
years was found. Only eight of 408 mushroom species occurred each composition can explain a large proportion of variation in the species
year on research plots. The production of mushrooms was correlated composition of fungal communities, even greater than soil properties.
with monthly sums of precipitation from June to October, while the time Similar results were obtained in Mediterranean forests, where fungi
of fruitbodies’ appearance was linked with mean temperatures in July species richness was positively correlated with tree species richness, and
and August (Straatsma et al., 2001). The high dependency of mushroom the tree host species identity was the main driver of the fungal com
production seasonality on weather conditions is visible in their response munity composition (Saitta et al., 2018). In China’s subtropical forest,
to climate change: the mushroom season now starts earlier and finishes the effect of tree species richness on fungi composition was examined on
later than several decades ago (Kauserud et al., 2010; Büntgen et al., a larger biodiversity scale (1–12 tree species). The study revealed that
2013; Kauserud et al., 2012). In spite of the longer period of sporocarp beta diversity of trees and fungi are strongly coupled. However, the ef
yielding, reports on the changes in mushroom production under the fects of tree species identity dominate over tree species richness on the
influence of climate change are contradictory, suggesting both increase diversity and composition of fungal communities (Chen et al., 2019).
or decrease, depending on the region (Büntgen et al., 2013; Yun and Similar results were also obtained by Otsing et al. (2021) in a boreal
Hall, 2004). forest in a study on EM fungi, which revealed that tree species identity is
Among other environmental characteristics, nitrogen concentration, an important determinant of species composition of the EM fungal
pH, type of soil, slope, and elevation are listed as main predictors of community. All these studies confirm the importance of tree species
mushroom production. The research carried out in the temperate forests identity and tree species richness for the development of fungal com
of the USA revealed that long-term deposition of nitrogen affects the munities. However, there are very few studies dealing with the impact of
fungi species composition, leading to an increase of saprotrophs pro these factors on mushroom yield. Most studies devoted to the factors
duction and a decrease of ectomycorrhizal fungi production (Morrison affecting mushroom production were conducted in Mediterranean and
et al., 2016). Other researchers confirmed the decline of mushroom boreal pine forests, which limited conclusions on tree species identity
production under high nitrogen concentrations (e.g.: Gillet et al., 2010). impact (Alday et al., 2017a; Karavani et al., 2018; Martínez de Aragón
The type of soil also matters, as fewer mushrooms are observed in soils et al., 2007; Pinna et al., 2010; Tahvanainen et al., 2016; Bonet et al.,
with decreasing proportion of sand (Taye et al., 2016). Soil acidity may 2010). Still, even in the studied pine monocultures, the impact of tree
have a contradictory influence on mushroom production, depending on identity was found. In the pre-Pyrenees forests of Spain, plots with
species or group of species in question. Production of some species (e.g. dominating Pinus sylvestris L. produce more mushrooms (60.26 kg ha− 1)
Lactarius sp.) increases with the acidity of the substrate (Taye et al., than those with dominating Pinus halepensis Mill. (15.17 kg ha− 1)
2016), while others (e.g. Tuber aestivum Vittad.) decrease (Bragato et al., (Martínez de Aragón et al., 2007).
2022). Additionally, in mountains in Mediterranean region, mushroom Bonet et al. (2004; 2008) revealed that mushroom production cor
production increases with increasing elevation (Bonet et al., 2008) but is relates with mushroom species richness. Similar result were obtained by
lower on the steeper and southern slopes (Bonet et al., 2010). Straatsma, Ayer, and Egli (2001) who showed positive relationship be
Forest management practices modify stand structure that has an tween yearly frequency of mushroom species and the average number of
influence on the diversity of trees (Poudyal et al., 2019), understory sporocarps. However, the evidence of direct linkage between tree spe
plants (Battles et al., 2001), and microbiota (Colombo et al., 2016), and cies composition and mushroom production is very limited. There is also
consecutively also the functioning of forest ecosystems. Thinning is the a knowledge gap on factors influencing mushroom production in mixed
most common silvicultural practice, however despite many studies there temperate forests, which have rarely been studied from this point of
are no clear conclusions on its impact on fungal communities. De-Miguel view. Taking into account the importance of fungi for human wellbeing
et al. (2014) showed that thinning positively affects the species and the functioning of forest ecosystems, we investigated factors
composition of fungal communities and their productivity, whereas affecting mushroom yield in Białowieża Primeval Forest (mixed
Parladé, Martínez-Peña, and Pera (2017) demonstrated negative temperate forest, northeastern Poland). We hypothesized that 1) tree
correlation of these factors. In the same time, some other studies did not species composition and tree species richness positively influence
reveal any effect of thinning on mushroom production and their species mushroom production via positive influence on fungal species richness.
richness (Salerni et al., 2020; Castaño et al., 2018). However, some Additionally, we assumed that 2) this relationship is stronger for ecto
researches indicate both increase (especially in the first years after mycorrhizal fungi than saprotrophic, as the relationship between living
thinning) and later decrease in fungal fruitbody production after trees and their mycorrhizal partners is more specific than between type
thinning (Tomao et al., 2017). of deadwood and saprotrophs, and also because trees provide their
Among basic tree stand characteristics, stand age, stand basal area, mycobionts access to carbohydrates, which may enhance the production
and canopy cover are most commonly reported to have the greatest of their sporocarps.
impact on mushroom production. Mushroom yield is higher in younger
stands, due to the faster growth rate of young trees (Tomao et al., 2017), 2. Methods
although the transition between this stage is fluid and depends on the
longevity of tree species and the fertility of the site (Martínez-Peña et al., 2.1. Study area
2012). In the mature forests, stand basal area is one of the best-studied
predictors of mushroom production, however, a study conducted in Our study was conducted in Białowieża Primeval Forest (approxi
Mediterranean pine forests suggests that stand basal area optimal from mately 1500 km2), one of the best preserved forests in Europe
2
K. Stojek et al. Forest Ecology and Management 522 (2022) 120451
(Jaroszewicz et al., 2019; Sabatini et al., 2018). This forest massif grzyby.pl and https://www.nagrzyby.pl), and a book, “Fungi of
stretches over the border between Poland and Belarus, in the eastern temperate Europe: Volume 1 + 2” (Laessoe and Petersen, 2019).
part of the Central European Lowland (52o41′ N; 23o49′ E) and covers
the flat plain with a mean altitude of 170 m a.s.l. (Sokołowski, 2004). It 2.4. Climate data
is a zone of warm-summer humid continental climate (Kottek et al.,
2006), with mean annual precipitation of 625 mm (for the period Custom-made microclimate stations were installed in 1- and 3-spe
1985–2015) and a mean annual temperature of 7.3 ◦ C (range from cies plots (n = 10) at the plot’s centre. During the whole sampling
5.9 ◦ C to 9.2 ◦ C, but since 1997, it has never dropped below 6.6 ◦ C) period, these continuously monitored air temperature, air humidity,
(Boczoń et al., 2018). black globe temperature and wind speed, with a sampling frequency of
Białowieża Forest lies in the zone of hemiboreal and mixed one hour. As the stations were not installed in all plots and measures
broadleaved-coniferous forests according to the European Environment displayed no noticeable differences among plots, we decided to use the
Agency classification (EEA, 2007). The western part of the forest (in the general meteorological data from Białowieża meteorological station
limits of Poland), where the study took place, is dominated by mesic and (52◦ 42′ 26′′ N 23◦ 50′ 53′′ E), located in the center of the forest. The hourly
mesotrophic habitats of mixed deciduous forests, with a high share of data of precipitation and daily mean, maximum and minimum tem
oak-lime-hornbeam forest (Tilio-Carpinetum type). Tree species domi peratures of air were downloaded from the website of The Institute of
nant in that part of Białowieża Forest include: Pinus sylvestris L. (27 %), Meteorology and Water Management (IMGW-PIB-2021).
Picea abies (L.) H.Karst (25 %), Alnus glutinosa (L.) Gaertn. (19,5%),
Quercus robur L. (12 %), Betula pendula Roth (8 %), Carpinus betulus L. (4 2.5. Forest stand data
%) and Fraxinus excelsior L. (3 %) (Sokołowski, 2004).
The plot-level forest inventory data for plots were obtained from
2.2. Sampling design FunDivEUROPE and Soil4Europe projects data portal (https://data.
botanik.uni-halle.de/fundiveurope). The data were gathered in 2012
In 2020 and 2021 we carried out mushroom monitoring on 20 plots and 2018 according to the methodology described by Jucker et al.
established for the needs of the EU-funded FunDivEUROPE project (2014) and included: tree species, diameter on breast height and wood
(https://project.fundiveurope.eu/) to study the effect of tree diversity increment (difference between wood biomass in 2012 and 2018).
on ecosystem multifunctionality. Within the project, 43 plots were set The soil pH, C/N ratio, nitrogen and carbon concentration were
up, which varied in terms of tree species richness (1–5 tree species) and measured in 2012 at the forest floor level (humus) and at the different
included Picea abies, Pinus sylvestris, Quercus robur, Betula pendula, and depth of mineral soil (0–10, 10–20, 20–30, 30–40 cm). Taking into
Carpinus betulus. The study plots were set in mature mixed deciduous account that most of fungal mycelia biomass is located in litter
forest of the oak-lime-hornbeam type (Tilio-Carpinetum) without signs of (forest floor) and the upper 10 cm of soil (Brabcová et al., 2016), we used
silvicultural activities for the last 10–20 years. All plots were located in our analysis data obtained for these two layers. Detailed procedure of
under similar environmental conditions (i.e. topography, geology, soil the measurements of soil variables was described in Dawud et al. (2016).
type) to minimize the influence of the variability of environmental The understorey cover was estimated in June 2020 using the six-step
factors on the subject of the study (Baeten et al., 2013). Each plot is 30 Braun-Blanquet cover-abundance method (Braun-Blanquet, 1928)
m × 30 m and is permanently marked in the field by wooden stakes at commonly used during plant surveys. The understorey was defined in
the corners to facilitate sampling. The plots are surrounded by a 10 m- this study as vegetation layer consisting of all herbaceous plants
wide buffering area with similar tree species composition and environ regardless of their height and trees and shrubs lower than 0.5 m.
mental conditions, which minimizes the edge effect of the surrounding
stands. 2.6. Statistical analysis
Due to intensive dieback of spruce during 2015–2018 (Kamińska
et al., 2020), all plots with spruce in the stand had been excluded from Prior to statistical analysis, in addition to taxonomic identification,
the monitoring of mushroom production to avoid the influence of the we categorized mushrooms for edible and non-edible (including
natural thinning of the stands. In effect, the investigation was carried out poisonous) and for ectomycorrhizal (EM), saprotrophic (SAP) and other
on 20 plots, encompassing four levels of tree diversity (1, 2, 3, and 4- properties (parasites or mushrooms with unclear/unidentified ecolog
tree species mixtures), including monocultures and mixtures of Pinus ical status). The online keys and atlases (https://www.grzyby.pl and
sylvestris, Quercus robur, Betula pendula and Carpinus betulus (not all https://www.nagrzyby.pl) and a book “Fungi of temperate Europe:
species combinations were present in the field and not all existing Volume 1 + 2” (Laessoe and Petersen, 2019) were used to classify
combinations had replication: Table S.1). mushrooms to each category. Factors influencing the species richness of
fungi were studied with the help of linear models (LM) implemented in
2.3. Monitoring of mushrooms the stats package (R Core Team, 2021). In all LMs, sums of mushroom
dry mass (total, EM, SAP) from all harvests on each plot were used as a
All plots were sampled every ten days for two years (2020, 2021), separate data record (n = 20). Since mushroom dry mass data were non-
from mid-June to the end of October (i.e. during the period of the normally distributed, we used the logarithmic scale to normalize their
highest intensity of production of sporocarps by edible species). We distribution. Akaike’s information criterion (AIC) was used to choose the
collected all mushrooms in the entire plot area, extended with a 2.5 m- best model (Akaike, 1973), using the MuMIn package (Bartoń, 2020). To
wide strip of the land around to enlarge the sampling area to 35 m × 35 estimate the contribution of each variable in a multivariate model we
m. We harvested sporocarps of all soil-dwelling and epixylic macrofungi, used hierarchical decomposition of goodness-of-fit measures of re
excluding bracket fungi and those with the size of the sporocarp < 0.5 gressions (hier.part) (Nally and Walsh, 2004).
cm. All mushrooms were brought to the laboratory for cleaning, fresh We used a t-test to check for the significance of differences in the
weight measurements, and species identification. After identification production of a specific group of mushrooms (SAP, EM, or total) be
and weighing we dried mushrooms in a food dehydrator at 50 ◦ C for tween the years.
about 24 h to eliminate errors of biomass estimation caused by varia Due to the low descriptive power of the LMs, we used Generalized
tions in the water content of fresh sporocarps, and weighed again with additive models (GAM) with integrated smoothness estimation from the
0.01 g accuracy. mgcv package (Wood, 2003; 2004; Wood, Pya, and Säfken. 2016; Wood,
We determined the mushroom species to the lowest possible level, 2011; 2017) to check the influence of climate factors on mushroom
using our expertise, available online keys and atlases (https://www. production between the years.
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K. Stojek et al. Forest Ecology and Management 522 (2022) 120451
To study how production changed between the years and how it and Russula cyanoxantha (Schaeff.) Fr. in 2021 but not in 2020
varied between the plots, we calculated the rate of collected mushroom (Table S.2).
biomass change between 2020 and 2021 in relation to mass in 2020 Out of all recorded mushroom species 116 were EM and 126 SAP.
((mass2021-mass2020)/ mass2020) for total, EM, and SAP biomass. Next, The remaining species were parasites or of unclear/unidentified
we built the LMs to explain the variation of changes between the plots. ecological status. Ninety-one species were edible.
All statistical analyses were carried out in R software version 4.1.2 (R During the two years of monitoring, we collected in total (from all
Core Team, 2021) using the RStudio version 2022.2.0.44 environment plots) 225.8 kg of mushrooms (fresh mass, mean 46.08 kg ha− 1 per
(RStudioTeam, 2022). year), including 134.4 kg (27.4 kg ha− 1 per year) of edible species,
which translated into 22.4 kg (4.6 kg ha− 1 per year) and 12.8 kg (2.6 kg
3. Results ha− 1 per year) of dry mass, respectively (Table S.3). EM species (14.4 kg
of dry mass (2.95 kg ha− 1 per year)) constituted 64 % of the total dry
Over a two-year study period we recorded 290 fungal species in total mass, whereas SAP 20.8 % (4.6 kg of dry mass (0.95 kg ha− 1 per year))
(149 species in 2020 and 238 in 2021), with 97 species recorded both (Table S.3).
years (Table S.2). Xerocomellus chrysenteron (Bull.) Šutara, Armillaria In both years the most productive species were Lactarius vellereus
mellea (Vahl) P. Kumm. and Mycena galericulata (Scop.) Gray were the (Fr.) Kuntze (1.82 kg and 1.81 kg of dry mass), Armillaria mellea (0.83 kg
most frequent species both years (present on at least 75 % of plots). and 1.45 kg), and Russula nigrescens (Bull.) Fr. (0,73 kg and 1.51 kg) in
Additionally Lycoperdon perlatum Pers. was very frequent in 2020 but 2020 and 2021, respectively. In 2021 Russula cyanoxantha was also
not in 2021 and Mycena vitilis (Fr.) Quél., Mycena rosella (Fr.) P. Kumm. highly productive (1.7 kg of dry mass) (Table S.2).
Fig. 1. Factors influencing the production of mushrooms in Białowieża Forest (North-Eastern Poland): A) all mushroom species (LM1), B) ectomycorrhizal species
(EM) (LM2), and C) saprotrophic species (SAP) (LM3); only significant interactions are displayed (Table 1; Table S.4; Table S.6–7).
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K. Stojek et al. Forest Ecology and Management 522 (2022) 120451
The total mushroom production in 2021 was 60 % higher than in 2020 and 2021 was + 75 % (±107(SD)). The EM mushroom production
2020 (m2020 = 3.5 kg ha− 1; m2021 = 5.6 kg ha− 1 of dry mass, respec changed by mean + 200 % (±322 (SD)). The enhancement of SAP
tively). The dry mass of EM mushrooms increased by 80 % (m2020 = 2.1 mushroom production was on the mean change level of + 18 % (±101
kg ha− 1; m2021 = 3.8 kg ha− 1), whereas dry mass of SAP fungi was (SD)) (Fig. S.1).
similar between the years (m2020 = 0.9 kg ha− 1; m2021 = 1 kg ha− 1) The change in total mushroom production in 2021 in comparison to
(Table S.3). 2020 (for all species) increased with increasing share of Quercus robur (t
= 4.935, p = 0.0004), pH of the soil at depth 0–10 cm (t = 2.806, p =
3.1. Effect of tree stand on mushroom production 0.02) and mushroom species richness (t = 3.358, p = 0.006), and with
decreasing nitrogen concentration in the soil (t = − 5.097, p = 0.0003),
We revealed high variability of mushroom production between the and decreasing plant species richness (t = − 3.561, p = 0.004) (Fig. 3A,
plots. Total mushroom production increased with increasing stand basal Table 1: LM7, Table S.11).
area (t = 5.822, p < 0.0001) (with optimal area estimated at 30–35 m2/ Higher increase in the production of EM mushrooms between the
ha) and mushroom species richness (t = 5.823, p < 0.0001), which years was observed in plots with a lower share of Pinus sylvestris (t =
turned out to be an essential variable, explaining around 35 % of vari − 2.296, p = 0.04) and Betula pendula (t = − 2.192, p = 0.05), lower plant
ation of mushroom production. The second most important value was species richness (t = − 2.800, p = 0.01), and higher tree density (t =
understorey cover negatively affecting sporocarps production (t = 4.067, p = 0.001) (Fig. 3B, Table 1: LM8, Table S.12). The bigger change
− 6.772, p < 0.0001) and explaining around 17 % of its variation. in SAP mushroom production was related to higher SAP species richness
Mushroom yield also increased with decreasing tree biomass increment (t = 2.162, p = 0.05) and lower tree species richness (t = − 3.322, p =
(t = − 4.777, p ≈0.0005) and share of Pinus sylvestris in the stand (t = 0.005) (the change was higher in monocultures and also increased with
− 5.182, p ≈0.0002) (Fig. 1A; Table 1: LM1; Table S.4; Table S.5). the share of Betula pendula in the stand) (Fig. 3C, Table 1:LM9,
The species richness of both EM and SAP mushrooms was the key Table S.13).
factor explaining 22 % of variation of EM mushroom production and 33
% of SAP production (t = 6.222, p = 0.0002; t = 3.552, p = 0.003, 3.4. Weather condition effects
respectively5 (Table S.5). Additionally, EM species production also
increased with increasing pH of the soil at depth 0–10 cm (t = 2.786, p In 2021, the sum of precipitation during the mushroom yielding
= 0.024), decreasing nitrogen concentration in the soil (t = − 3.720, p = period was higher than in 2020 (324 mm and 251 mm, respectively),
0.006), and decreasing understorey cover (t = − 2.314, p = 0.05) especially in July, when the monthly rainfall in 2021 was over two times
(Fig. 1B; Table 1: LM2, Table S.6). The production of SAP fungi was higher than the year before (142.7 mm vs 67.2 mm, respectively). The
negatively influenced by canopy cover (t = − 2.479, p = 0.03) (Fig. 1; mean monthly air temperature of the yielding period did not differ be
Table 1:LM3, Table S.7). tween the years (t-test; t = 0.64032, p-value = 0.534; temp2020 = 16.29
± 3.85(SD)◦ C, temp2021 = 15.78 ± 5.44(SD)◦ C).
3.2. Effects of tree stand on mushroom species richness The gamma models revealed that in 2021 total mushroom produc
tion depended on the sum of precipitation from the month preceding the
The total species richness of mushrooms was not explained by any month of mushroom collection (i.e. the period 60 to 30 days before the
stand characteristics (Table 1: LM4, Table S.8). However, species rich date of sampling) but not on the temperature. In 2020 the mean tem
ness of EM mushrooms increased with increasing forest floor pH (t = perature of the ten days before sampling explained mushroom produc
5.764, p < 0.0001), plant species richness (t = 4.528, p = 0.0007), stand tion, but not the precipitation (Fig. 4; Table 2.).
basal area (t = 3.930, p = 0.002), carbon to nitrogen ratio of the humus
layer (t = 4.458p = 0.0008), tree species richness (t = 2.199, p = 0.05), 4. Discussion
and share of Carpinus betulus in the stand (t = 3.398, p = 0.005). It also
decreased with increasing cover (t = -4.244, p = 0.001) (Fig. 2A, In our study we investigated factors affecting mushroom yield,
Table 1: LM5, Table S.9). Among them, pH, C/N ratio, and plant species mushroom species richness, and stability of mushroom production be
richness were essential factors explaining 22 %, 16 % and 15 % of tween years. Due to scrupulously selected plots (similar topology, ge
variation, respectively (Table S.5). The rest of the factors were less ology, soil type; lack of thinning; stand’s maturity) (Baeten et al., 2013),
important and each of them explained less than 10 % of variation of EM we minimized the influence of environmental factors other than stand
species richness explained by the model (Table S.5). SAP species rich characteristics and weather conditions. Therefore, tree stand composi
ness was influenced only by the pH of the soil at depths 0–10 cm (t = tion should pose a prevailing impact on the functioning of the studied
− 2.858, p = 0.01) (Fig. 2B, Table 1: LM6, Table S.10). mushroom community. However, plots also differed in terms of other
variables affected by tree stand characteristics like understorey cover, N
3.3. Year effects concentration and pH (Ampoorter et al., 2016; Dawud et al., 2016).
The mean mushroom production differed between the 2020 and
The mean change of the total mushroom production per plot between 2021, which is consistent with the previous studies revealing high
Table 1
Linear models explaining mushroom production (LM1-3), species richness (LM 4-6), and differences in mushroom productivity between years (LM7-9) for all
mushrooms (LM1, LM4, LM7), EM mushrooms (LM2, LM5, LM8) and SAP mushrooms (LM3, LM6, LM9).
Model Residual standard error: Degrees of freedom Multiple R-squared: Adjusted R-squared: F-statistic p-value
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K. Stojek et al. Forest Ecology and Management 522 (2022) 120451
Fig. 2. Factors influencing A) ectomycorrhizal (LM5) and B) saprotrophic mushrooms species richness (LM6) in Białowieża Forest (North-Eastern Poland); only
significant interactions are displayed (Table 1; Table S.9 and S.10).
variation of mushroom biomass between years (Büntgen et al., 2013; Even in similar climate zones and time scales the differences are high.
Alday et al., 2017a). The overall productivity revealed in our study is Alday et al. (2017a) collected around 130 kg ha− 1 mushrooms per year,
difficult to compare with other studies due to varied yielding times, whereas Martínez de Aragón et al. (2007) reported several times lower
groups of mushrooms included in analysis and forest characteristics like annual sporocarp production, around 29.4 kg ha− 1, despite the fact that
its management, continuity of forest cover or naturalness of ecosystem. both studies were carried out in the Mediterranean climate zone with
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K. Stojek et al. Forest Ecology and Management 522 (2022) 120451
Fig. 3. Factors influencing A) all mushroom; B) ectomycorrhizal; C) saprotrophic mushroom production relative mean change between 2021 and 2020 in Białowieża
Forest (North-Eastern Poland); only significant interactions are displayed (Table 1, Table S.11-S.13).
weekly harvesting from the beginning of September to the end of From the point of view of mushroom production, the optimal stand basal
December. Our research was conducted in the temperate climate zone area (resulting in the maximal mushroom yield) varies in the literature
and in one of the most natural forest ecosystems in Europe, character between 10 and 40 m2/ha, depending on the study region, dominant
ized by high species richness of mushrooms (Jaroszewicz et al., 2019). tree species and soil properties, and can be different for specific mush
Our results suggest that high species richness of fungi should enhance room species (Tomao et al., 2017). In our study, in the European mixed
the mushroom production, however, the mean production in our study temperate forest, the stand basal area yielding the highest mushroom
(46,08 kg ha− 1 per year) was similar to results obtained by Martínez de production was estimated at 30–35 m2/ha. That is similar to the 35–40
Aragón et al. (2007) from the Mediterranean zone. m2/ha suggested by Sánchez-González et al. (2019) based on studies
carried out in Pinus sylvestris and Pinus pinaster Aiton stands in Northern
Spain.
4.1. Factors influencing mushroom production Our analyses revealed a decrease of mushroom yield with increasing
tree increment (i.e. wood biomass production). This is the opposite of
Close to 95 % of variation in mushroom production was explained by what was reported by Collado et al. (2019), who found a positive
stand characteristics (Table S.5). Stand basal area was one of the main interaction of tree growth and mushroom yield in the Mediterranean
factors affecting mushroom yield, which is consistent with papers from region. This positive interaction was explained by the higher amount of
Mediterranean forests (Martínez-Peña et al., 2012; Bonet et al., 2010).
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K. Stojek et al. Forest Ecology and Management 522 (2022) 120451
Fig. 4. Relationship between weather conditions and mushrooms production in Białowieża Forest in 2020 and 2021. A, B – sum of precipitation from the month
preceding the month of mushroom collection; C, D - mean temperature of the ten days before mushroom collection.
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accounted for close to 10 % of the dry mass of all collected mushrooms. be just to low to affect SAP production, whose optimum is much higher.
Armillaria fungi are both facultative saprophytes and forest pathogens The observed linkage between P. sylvestris and mushroom production
(Roll-Hansen, 1985), often affecting weakened trees and causing their could be very local, as the impact of tree species identity often has a local
death. Thereby, the stronger the trees, the lower sporocarp yield of this character, not extending too far beyond the crown or root range. This
species. In our opinion, even with a 10 % share in the total yield, this explains the importance of share of this tree species for mushroom
species, in combination with saprotrophs, can change the lack of impact production: the more pines, the bigger the share of the plot area, char
of tree growth on mushroom yield, observed in temperate forests by acterized by conditions not optimal for fungi. Adamo et al. (2021)
Collado et al. (2019), to a negative one revealed by us. demonstrated that mushroom yield does not differ between the studied
In our study, mushroom production was also negatively affected by pine species (P. sylvestris, P. halepensis, P. nigra Arn), which may be
understorey cover. A similar effect was observed in Finland in the case of caused by the similar acidifying effect of all these species. However,
Tricholoma matsutake S. Ito & S. Imai. Production of this mushroom Martínez de Aragón et al. (2007) showed that in P. sylvestris stands
decreased with density of understorey vegetation (Vaario et al., 2013), mushroom production is higher than in P. halepensis and P. nigra stands.
which was explained as an effect of several factors – light availability, The different results of this study may have been caused by variation of
inhibition of development of mycelium by herbs, and higher competi soil properties and other stand characteristic between plots not taken to
tion between plant roots and fungi. High understorey cover limits light account in the study, limiting the impact of trees to the local scale.
availability, which is necessary for the development of fruiting bodies
(Sakamoto, 2018). Gramss (1985) also proved that decaying grasses 4.2. Factors affecting species richness of fungi
partly inhibit the growth of the mycelium, which can negatively affect
mushroom production. Additionally, a denser understorey causes higher In our study, the production of all the studied groups of mushrooms
root competition (Coomes and Grubb, 2000), which means higher (EM, SAP but also total) was positively related to the species richness of
fungal competition for limited soil resources. fungi. This is consistent with Bonet et al., 2004 and Bonet et al., 2008),
Soil nitrogen concentration negatively influenced EM mushroom who demonstrated similar links for many functional groups of mush
yield, which was consistent with earlier observations (Buée et al., 2011) room: all, edible, marketed edible, Lactarius spp. In our study fungal
and experiments (Gillet et al., 2010). Many studies have shown that high species richness was the key factor, explaining around 35 % of variation
nitrogen levels reduce EM mycelium growth, decrease their species di of mushroom production (Table S.5, Table 1. (LM1)). The importance of
versity, and reduce sporocarp production, whereas SAP fungi are much this factor prompted us to find out which stand characteristics influence
less affected (Lilleskov et al., 2001; Peter et al., 2001; Hasselquist and this variable.
Högberg, 2014). The difference is probably caused by diverse ways of The model explaining the species richness of all mushrooms did not
carbon acquisition by these two groups of fungi. High nitrogen avail reveal any factors affecting this variable. This is probably because
ability in the soil causes a reduction in the allocation of carbon to the different factors affect specific fungi species in ways contradictory to
roots by trees, which limits C supply for EM mushrooms (Demoling each other, and one may also expect many factors influencing just very
et al., 2008). SAP obtain carbon from dead biological matter, which specific species or species groups, like availability of spore vectors or
decay rates increase with increased availability of nitrogen (Rinne et al., high substrate specialization of fungi, etc. However, in the case of EM
2017). mushrooms, their species richness depended mainly on soil properties
Tree species composition did not affect total mushroom production (pH of the forest floor explained 22 % of variation and C/N 16 % of
on our study plots, which is contrary to our expectations based on the variation; Table 1. (LM5); Table S.5) and some stand characteristics –
fact that at least mycorrhizal fungi are very often tree species specific. plant species richness, stand basal area, understorey cover, tree species
Only the share of Pinus sylvestris negatively impacted their yield. In plots richness and share of Carpinus betulus. Our results were consistent with
with a higher share of pine, the biomass of mushrooms was lower than in reports of Tedersoo et al. (2016) and Chen et al. (2019) describing soil
plots with a lower share, whereas the yield of mushrooms in plots properties as key drivers of fungal species richness.
without pine varied but did not show any detectable trends. Most studies Plant species richness and their cover also turned out to be important
on mushroom production have been conducted in pine-dominated factors explaining 15 % and 8 % (respectively) of richness of EM
Mediterranean (Martínez-Peña et al., 2012; Karavani et al., 2018; mushrooms (Table 1. (LM5); Table S.5), which is consistent with the
Salerni et al., 2002) and boreal forests (Pinna et al., 2010; Tahvanainen report of Hiiesalu, Bahram, and Tedersoo (2017), who suggested that
et al., 2016), which did not allow an assessment of the importance of this plant species richness and their productivity may be the key factor
tree species in comparison to others. A positive influence of an admix explaining the diversity of fungi.
ture of another tree species in pine stands on fungal species richness was In our research, forest monocultures were characterized by lower EM
found by Suz et al. (2017), who compared fungal communities of pine mushroom species richness than mixed stands, which slightly increased
and pine-oak stands in Finland. Pure pine stands hosted on average 26 with increasing tree species richness. This is consistent with studies
fungi species, while oak admixture increased their species richness to 38 suggesting the positive influence of tree diversity on the species richness
species, but the authors did not take into account the exact share of pine of fungi (Saitta et al., 2018; Chen et al., 2019), and the study by Suz et al.
in the studied stands. In our study, increasing abundance of P. sylvestris (2017), reporting higher numbers of species of fungi in Q. robur – P.
in stands negatively affected the yield of all mushrooms. In our opinion, sylvestris forest than in a P. sylvestris monoculture. Additionally, we
this negative influence was mediated via litter and soil/substrate acid revealed that the share of Carpinus betulus also positively affected
ity. Pine is one of the species which has an acidifying effect on forest mushroom species richness, but only to the 30 % share of the basal area
soils (Achilles et al., 2021), which negatively impacts mushroom pro of all trees. The positive effect of C. betulus may be a result of its
duction. Yamanaka (2003) found that higher pH of the substrate posi expansion in Białowieża forest and the high share of very young trees of
tively influences the production of many mushrooms, with the optimum this species under a canopy of mature-dominant trees of other species,
at pH = 5–6 for EM and at pH = 7–8 for SAP mushrooms, while reaction which can cause accelerated transport of nutrients to mycelium and
of the pine litter is much lower (pH ≈ 4) (Smal and Olszewska, 2008). higher EM mushroom production.
Our analysis revealed a similar positive relation between the pH of the The saprotrophic mushroom species richness was negatively affected
soil and production of EM mushrooms, but lack of it for SAP mushrooms by pH of the soil at depth 0–10 cm, which is in contradiction with reports
(only negative effect on SAP species richness). As pH gradient of soil at from Amazonian forests, where Queiroz et al. (2021) found a direct,
depth 0–10 cm was very short (3.5–4.5), the impact of pH on EM pro positive impact of pH on the species richness of saprotrophic fungi. The
duction could be more visible as their optimum is closer to the tested difference may be caused by the short gradient of measured pH (lack of
interval, whereas the differences between pH around 3.5 and 4.5 could positive impact of higher pH) and the influence of high inhibition of
9
K. Stojek et al. Forest Ecology and Management 522 (2022) 120451
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K. Stojek et al. Forest Ecology and Management 522 (2022) 120451
the very short research period (two seasons) or by fact that in our study Alday, J.G., Bonet, J.A., Oria-de-Rueda, J.A., Martínez-de-Aragón, J., Aldea, J., Martín-
Pinto, P., de-Miguel, S., Hernández-Rodríguez, M., Martínez-Peña, F., 2017a. Record
we defined mushroom species richness as the species richness of fruiting
breaking mushroom yields in Spain. Fungal Ecol. 26 (April), 144–146. https://doi.
mushrooms and not all of the fungi present on plots. This aspect requires org/10.1016/j.funeco.2017.01.004.
further research with the use of molecular techniques, allowing the Alday, J.G., Martínez de Aragón, J., de-Miguel, S., Bonet, J.A., 2017b. Mushroom
determination of the total fungal diversity of forest soils and methods biomass and diversity are driven by different spatio-temporal scales along
mediterranean elevation gradients. Sci. Rep. 7 (1), 45824. https://doi.org/10.1038/
allowing estimation of the total biomass of soil dwelling mycelia. This srep45824.
topic is also worth exploration due to the role of fungi in the bonding and Alexe, A.N., 1964. Pinus sylvestris. Pinus sylvestris. https://www.cabdirect.org/cabdirec
depositing of carbon in forests soils (Clemmensen et al., 2013). t/abstract/19645605476.
Ampoorter, E., Federico, S., Harald, A., Lander, B., Sigrid, B., Elisa, C., Andrea, C., et al.,
2016. Driving mechanisms of overstorey-understorey diversity relationships in
Funding European forests. Perspect. Plant Ecol., Evol. System. 19 (April), 21–29. https://doi.
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Atkinson, M.D., 1992. Betula Pendula Roth (B. Verrucosa Ehrh.) and B. Pubescens Ehrh.
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Forest project, funded through the 2018–2019 BiodivERsA joint call for Bååth, E., Anderson, T.-H., 2003. Comparison of soil fungal/bacterial ratios in a PH
research proposals, under the BiodivERsA3 ERA-Net COFUND pro gradient using physiological and PLFA-based techniques. Soil Biol. Biochem. 35 (7),
955–963. https://doi.org/10.1016/S0038-0717(03)00154-8.
gramme, and with the funding organisations of the Polish National Baeten, L., Verheyen, K., Wirth, C., Bruelheide, H., Bussotti, F., Finér, L., Jaroszewicz, B.,
Science Centre - NCN (project no. 2019/31/Z/NZ8/04032), DFG (Ger et al., 2013. A novel comparative research platform designed to determine the
many), ANR (France), FWO (Belgium) and FWF (Austria). functional significance of tree species diversity in European forests. Perspect. Plant
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Declaration of Competing Interest Norway Spruce Stands. Water 10 (11), 1502. https://doi.org/10.3390/w10111502.
Bonet, J.A., Fischer, C.R., Colinas, C., 2004. The relationship between forest age and
aspect on the production of sporocarps of ectomycorrhizal fungi in pinus sylvestris
The authors declare that they have no known competing financial forests of the central Pyrenees. For. Ecol. Manage. 203 (1), 157–175. https://doi.
interests or personal relationships that could have appeared to influence org/10.1016/j.foreco.2004.07.063.
the work reported in this paper. Bonet, J.A., Palahí, M., Colinas, C., Pukkala, T., Fischer, C.R., Miina, J., Martínez de
Aragón, J., 2010. Modelling the production and species richness of wild mushrooms
in pine forests of the central pyrenees in Northeastern Spain. Can. J. For. Res. 40 (2),
Data availability 347–356. https://doi.org/10.1139/X09-198.
Bonet, J.A., Pukkala, T., Fischer, C.R., Palahí, M., Aragón, J.M., Colinas, C., 2008.
Empirical models for predicting the production of wild mushrooms in scots pine
Data will be made available on request. (Pinus Sylvestris L.) forests in the central pyrenees, 206–206 Ann. Forest Sci. 65 (2).
https://doi.org/10.1051/forest:2007089.
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