10.6092/issn.2531-7342/16464
Climate change can affect forest ecosystems, especially through an increase of extreme events. In order to verify whether mycosilvicultural practices could mitigate the effects of climate change, productivity of Boletus edulis in Abies alba managed plantations was correlated to intense rainfall and temperature peaks during three years. Fungal productivity in each of the 21 days following an extreme climatic event was considered. Results showed that sudden increases in maximum temperature seemed to have an inhibitory effect on B. edulis productivity in sites with no or modest thinning. In sites with heavy thinning, productivity seemed to be favoured by high temperatures, starting from the twentieth day following the extreme event. Mycosilviculture may mitigate the climate change effects; however, further studies are needed to verify how climate-dominated effects can be altered by local factors and how ecological relationship between B. edulis and forest ecosystem will be affected.
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Combined impact of forest management and climate change on <em>Boletus edulis</em> productivity: may mycosilviculture mitigate the effects of climate extremes?
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Zubaidi MA, Proch J, Konieczny P, Tomczyk Ł (2021) Toxicity testing by the microbial assay for risk assessment (MARA) in relation to trace elements content in King Bolete (Boletus edulis) collected in several sites of Poland. Applied Sciences 11(9):4166. https://doi.org/10.3390/app11094166
Combined impact of forest management and climate change on <em>Boletus edulis</em> productivity: may mycosilviculture mitigate the effects of climate extremes?
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                   IJM - Italian Journal of Mycology
                   ISSN 2531-7342 - Vol. 52 (2023): 76-88
                   Journal homepage: https://italianmycology.unibo.it/

Research article

     Combined impact of forest management and climate change on
     Boletus edulis productivity: may mycosilviculture mitigate the
                      effects of climate extremes?

                                Elena Salerni1, Luca Paoli2, Claudia Perini1
1
    Department of Life Sciences, University of Siena, Via Mattioli 4, 53100 Siena, Italy.
2
    Department of Biology, University of Pisa, Via Ghini 13, 56126 Pisa, Italy.

Corresponding author e-mail: elena.salerni@unisi.it


Article info
Received 16/2/2023; accepted 4/4/2023
https://doi.org/10.6092/issn.2531-7342/16464

Abstract
Climate change can affect forest ecosystems, especially through an increase of extreme events. In order to
verify whether mycosilvicultural practices could mitigate the effects of climate change, productivity of Boletus
edulis in Abies alba managed plantations was correlated to intense rainfall and temperature peaks during
three years. Fungal productivity in each of the 21 days following an extreme climatic event was considered.
Results showed that sudden increases in maximum temperature seemed to have an inhibitory effect on B.
edulis productivity in sites with no or modest thinning. In sites with heavy thinning, productivity seemed to be
favoured by high temperatures, starting from the twentieth day following the extreme event. Mycosilviculture
may mitigate the climate change effects; however, further studies are needed to verify how climate-dominated
effects can be altered by local factors and how ecological relationship between B. edulis and forest ecosystem
will be affected.

Keywords
ectomycorrhizal fungi, wild edible mushrooms, coniferous plantations, extreme precipitation, extreme
temperature, forest thinning, Italy


Introduction

The Boletus edulis species complex (penny bun mushroom, cep, cèpe de Bordeaux, porcino, Steinpilz)
includes four European species (Boletus edulis Bull., Boletus aereus Bull., Boletus pinophilus Pilát
& Dermek and Boletus reticulatus Schaeff.) whose molecular identification is based on ITS specific
primers developed by Mello et al. (2006). They are rich in dietary minerals, like sodium, iron, calcium,
and magnesium and have therapeutic effects, which are useful in preventing many health issues due
to their antibacterial, antimutagenic and antiviral activities (Zubaidi et al., 2021).
    The Boletus edulis species complex belongs to ectomycorrhizal (ECM) fungi producing edible
mushrooms highly prized worldwide (Boa, 2004; Bonet et al., 2010; Martínez-Peña et al., 2012a;
García-Bustamante et al., 2021), associated with various trees and shrubs (Fagales, Malvales,
Malpighiales, Ericales, Pinales, ecc.). These fungal species are collected exclusively from wild
(Cannon and Kirk, 2007), and their cultivation is a challenging target for many agro-food biotech

Department of Agricultural and Food Science in partnership with the Italian Mycological Society (UMI).
The journal is hosted and maintained by ABIS-AlmaDL. © 2023 The Authors. This work is licensed under CC BY 4.0
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companies. Up to now, a major problem is that only a few ECM fungal species can be induced to
fruit in co-culture in interaction with their hosts. These difficulties, the socio-economic relevance
of mushrooms picking (e.g., Bonet et al., 2010; Alonso Ponce et al., 2011; Martínez de Aragón et
al., 2011; Martínez-Peña et al., 2012b; Diez et al., 2013; Leonardi et al., 2017) coupled with the
low profitability of timber production is driving a change in forest management paradigms and
practices, switching from traditional forest planning focused on timber production to more complex
multifunctional silvicultural schemes (e.g., Salerni and Perini, 2004; Palahí et al., 2009; Bonet et al.,
2012; Pierangelo and Rolland, 2013; Lin et al., 2015; Cantiani, 2016; Leonardi et al., 2017; Salerni et
al., 2020). One of these practices is the so-called “mycosilviculture”, which attempts to integrate timber
and mushroom production (Martínez-Peña et al., 2011). Sound forest planning for the joint production
of wood and mushrooms requires knowledge of both mushroom ecology and forestry techniques
useful for wood production (Palahi et al., 2009). In general, the main factors affecting mushroom
production are local site characteristics (e.g., altitude, exposition, slope, soil characteristics), stand
structure (e.g., tree species composition, stand density and age, basal area, standing volume, mean
height), climatic variables (e.g., precipitation, temperature, CO2 concentration) and anthropogenic
factors (e.g., pollution, forest management). Land plot basal area (Salerni and Perini, 2004; Martínez-
Peña et al., 2012b), age category (Salerni and Perini, 2004; Martínez-Peña et al., 2012b), rainfall
(Salerni and Perini, 2004; Parladé et al., 2017; García-Bustamante et al., 2021) and air temperature
(Hernández-Rodríguez et al., 2015) have been identified as some of the relevant factors influencing
B. edulis basidioma production.
    Human influence on the climate system is evident: as a known example, recent anthropogenic
emissions of greenhouse gases reached the highest peaks in history. By 2100, the atmospheric
concentration of CO2 is predicted to rise between 540–970 ppm above the current concentration.
Together with other greenhouse gases such as CH4, this may lead to a predicted global increase of
temperatures from 1.1 °C up to 6.4 °C, depending on different predictive models used and the region
of the world concerned (IPCC AR4, 2007). As a reciprocal consequence, recent climate change has
widespread impact on humans and natural systems (IPCC AR5, 2014) and thus, the interest in its
mutations on a large and local scale has expanded far beyond the scientific community. There are
evidences that a negative influence on the production of mushrooms can be attributed to global
climate change and local effects on the alteration of climatic parameters, also in the Mediterranean
area (Kauserud et al., 2012; Boddy et al., 2014; Büntgen et al., 2015; Ágreda et al., 2015; 2016).
The IPCC AR5 report (2014) underlines how climate change has affected climatic extremes and,
in the future, the severity and frequency of extreme events are expected to be exacerbated. In the
Mediterranean area, according to the report aimed at identifying and evaluating the extent of variations
in climatic extremes in Italy over the last half century (Fioravanti et al., 2013), all parameters linked
to temperature extremes show a warming trend, while less marked are those associated with the
reduction of extremes of cold. Concerning precipitation extremes, an increase in intense rainfall is
reported especially in southern Italy and on the islands.
    In the present paper, a previously collected dataset (Salerni and Perini, 2004) was updated and
reworked in order to verify whether mycosilvicultural practices are able to mitigate the effects of
the variability of climatic parameters, especially those related to temperature and rainfall. For this
reason, data related to the productivity of B. edulis in managed plantations of Abies alba Mill. were
investigated in relation to precipitation events and temperature peaks occurred during the sampling
period.



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Material and Methods

The study was carried out in artificial fir woods of Mt. Amiata in the municipality of Abbadia San
Salvatore (Siena, Italy) (42°51’57’’N, 11°39’03’’E, mean elevation 1,050 m a.s.l.). Mt. Amiata is
an isolated outcrop (1,738 m a.s.l.) in southern Tuscany, consisting of volcanic rocks deposited on
allochthonous substrates of Cretaceous and early Cenozoic Ligurian facies (Giannini et al., 1972).
The study sites are in the petrographic province of quartz porphyrites of ignimbrites (Carta Geologica
d’Italia, 1965). Mean annual temperature is 11.4 °C (max: 27.2 °C in August; min: 5.9 °C in January).
Mean annual rainfall is 1,210 mm, with November as the rainiest month (Centro Funzionale Regione
Toscana: http://www.sir.toscana.it). Further information on the study sites is reported in Salerni
and Perini (2004). The plantation is dominated by 33-year-old A. alba, followed by a minority of
Picea abies (L.) H. Karst. and clusters of Pinus nigra J.F. Arnold and broadleaved trees such as Acer
monspessulanum L., Castanea sativa Mill. and Prunus avium (L.) L. (Salerni and Perini, 2004).
   Mycological observations were made in 36 plots (each one of 250 m2) in three different woody
areas (12 plots each) and very close to each other. In 1999, one third of the plots was subjected to
medium thinning, one third to heavy thinning and one third considered as a control with no thinning.
Based on the principal dendrometric approach (Salerni and Perini, 2004), the thinning was carried out
taking tree base area (G m2 ha-1) as standard. In this study a mean removal of 20% of trees with respect
to the standard area is intended as medium thinning, while removal of 40% as a heavy one. Around
each plot, buffer areas were marked out. Furthermore, in half of the plots for each forest treatment (n
= 6), the litter layer was manually removed to assess the effects of dead plant organic material present
on top of the mineral soil surface on the fungal fruiting process (Fig. 1).




         Fig. 1 - Experimental design realized in the study areas.




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   Data on occurrence of basidiomata of B. edulis species complex in the study sites were gathered
for 3 years (2000–2002) after forest management. The data of 2002 were elaborated for the first
time in this study, while those of 2000 and 2001 were retrieved from Salerni and Perini (2004).
Observations were made on daily basis by local mycologists during major fruiting periods (mostly
August–November). During each survey, all basidiomata of B. edulis s.l. were collected to simulate
what happens during the harvest period and then counted.
   To assess climate influence on the fruiting process of B. edulis s.l., climatic parameters were
obtained from a nearby weather station (Santa Fiora), 7 km away from the study sites. A primary
dataset consisted of daily averages of air temperature and vertical atmospheric precipitation.
Primary data were subsequently summarized as means, minimum and maximum values of monthly,
seasonal and annual rainfalls and temperatures. Moreover, since it is indicated that extreme climatic
events may cause serious consequences on the environment, additional climatic parameters were
selected following the recommendations of the Expert Team on Climate Change Detection and
Indices (ETCCDI) of the CLIVAR Working Group on Climate Change Detection (Commission for
Climatology of the World Meteorological Organization), who has defined a set of 27 indices suitable
for describing the extremes of temperature and precipitation in terms of frequency, intensity and
duration (Fioravanti et al., 2013). Among these, the index for precipitation (R20 - number of days
with very intensive precipitation, i.e. ≥ 20 mm) and two absolute temperature indices (TXx – maxima
of daily maximum temperature; TNn - minima of daily minimum temperature) were selected for this
study. Correlations between values of climatic parameters and number of basidiomata were analysed
by Pearson’s linear coefficient.

Results

In the period 2000–2002, basidiomata of two species of B. edulis complex were collected: B. edulis
sensu stricto was abundantly occurring in the study area, while the sporadic findings belonging to B.
pinophilus reported only six times in three years were here not considered. The number of basidiomata
increased in all sampling sites during the study period (Fig. 2). In those plots where the litter was
removed, the number of basidiomata was lower in comparison with litter present plots (Fig. 2).
    The highest increase in production was observed in areas subjected to medium thinning where the
litter was maintained (Fig. 2b). Compared to the control (Fig. 2a), the number of basidiomata decreased
by about one third in the areas treated by heavy thinning (Fig. 2c). The number of basidiomata found
in relation to mean monthly temperature and total monthly rainfall is shown in Figure 3.
    During the first two years of the study, the maximum productivity was recorded during autumn,
in particular in October (338 basidiomata in 2000 and 584 in 2001), while in the following year, the
maximum production (574 basidiomata) shifted in August, two months earlier. This trend is in line
with values of mean monthly temperatures. In the first two years, the highest temperatures were
measured in August, while in 2002 in June, followed by a rainy sum0mer (Fig. 3). Table 1 shows the
values of these variables calculated both annually and seasonally for all three years of study.




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                  Fig. 2 - Total count of B. edulis basidiomata in all plots subjected to different
                  silvicultural treatment - control no thinning (a), medium thinning (b), heavy
                  thinning (c) - during the study period (2000-2002). In each treatment, half plots
                  were subjected to litter removal, N = 12.


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                  700                                                                                          25
                                                    P mm           Boletus edulis           Tmed

                  600
                                                                                                               20

                  500




                                                                                                                    Temperature°C
                                                                                                               15
  Rainfall (mm)




                  400


                  300
                                                                                                               10


                  200

                                                                                                               5
                  100


                    0                                                                                          0
                         01/2000
                         02/2000
                         03/2000
                         04/2000
                         05/2000
                         06/2000
                         07/2000
                         08/2000
                         09/2000
                         10/2000
                         11/2000
                         12/2000
                         01/2001
                         02/2001
                         03/2001
                         04/2001
                         05/2001
                         06/2001
                         07/2001
                         08/2001
                         09/2001
                         10/2001
                         11/2001
                         12/2001
                         01/2002
                         02/2002
                         03/2002
                         04/2002
                         05/2002
                         06/2002
                         07/2002
                         08/2002
                         09/2002
                         10/2002
                         11/2002
                         12/2002
  Fig. 3 - Mean monthly temperature (Tmed), total monthly rainfall (P mm) and total monthly number of B. edulis
  basidiomata in the study period (2000-2002).

Table 1 - Summary of climatic parameters on seasonal basis during the study period (2000‒2002) (RT - number of rainy
days; Tmax - maximum temperature; Tmin - minimum temperature; Tmean - mean temperature; TXx - maxima of daily
maximum temperature; TNn - minima of daily minimum temperature; R20 - days with intensive precipitation, i.e. ≥ 20
mm). Annual referred to the time range between 1st January and 31st December; while winter, spring, summer and autumn
referred to the first and the last day of each season in the traditional Gregorian calendar, respectively.

                                  RT        T max   T min   T mean R20              TXx      TNn
                                  n. days   (°C)    (°C)    (°C)       n. days      (°C)     n. days   (°C)    n. days
                  2000   Annual   122       16.07   7.65    12.29      14           20.43    125       2.62    82
                         Winter   18        7.93    0.81    4.61       1            11.67    5         -4.57   3
                         Spring   33        17.63   8.72    13.65      2            21.55    21        3.65    10
                         Summer   20        25.36   13.88   20.21      1            28.03    21        9.68    8
                         Autumn   43        13.51   7.22    10.78      6            18.60    9         4.25    17
                  2001   Annual   87        16.66   7.87    12.26      12           22.02    86        2.72    67
                         Winter   15        8.83    2.40    5.61       3            14.00    1         -4.00   4
                         Spring   33        16.67   7.88    12.28      4            21.83    12        3.45    15
                         Summer   13        25.16   13.70   19.43      1            28.53    18        9.18    9
                         Autumn   22        13.31   5.80    9.55       3            18.10    26        1.15    14
                  2002   Annual   126       15.54   7.59    11.57      14           20.52    96        2.80    70
                         Winter   17        8.91    1.59    5.25       2            14.83    9         -1.77   10
                         Spring   32        17.09   7.78    12.44      2            23.33    9         3.05    12
                         Summer   27        23.39   13.82   18.60      6            27.75    9         10.35   6
                         Autumn   44        14.11   7.46    10.78      4            16.63    11        2.08    17


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    During the study period, about 12% of rainy days were characterized by very intense precipitation
(R20 ≥ 20 mm). These events concerned in particular way the productive seasons of B. edulis (as
said above autumn 2000-2001 and summer 2002), where the percentage of days with R20 ≥ 20 mm
increased by 14% (6 days out of 43 in the 2000 and 3 days out of 22 in 2001) and over 20% (6 days
out of 27 in 2002) (Table 1). In 2000, the annual TXx value (20.43 °C) was exceeded for 125 days,
and in particular, during autumn 2001, the TXx value (18.10 °C) was exceeded for 26 days (Table 1).
    To verify whether and how the various silvicultural treatments affected the productivity of B. edulis
in relation to the selected climatic parameters, a correlation analysis (linear Pearson coefficient) was
performed between the productivity of B. edulis observed in the different pattern of treatments in each
of the 21 days following an extreme climatic event (R20, TXx and TNn) and the climatic values of the
same extreme events during the overall study period. The results, with 12 days with significant values
out of 21 considered, are shown in Table 2.
    In the case of very intense rain phenomena (R20 ≥ 20 mm), the rainfall had a positive effect on
the productivity of B. edulis, in particular on the twelfth day following the event (Table 2). Most
of significant values, here presented, are in areas where the litter layer was not removed. In plots
subjected to medium intensity thinning, this positive effect was also observed on the second day. On
the contrary, in plots where the thinning was more intense heavy rains seemed to have an inhibitory
effect on species productivity the thirteenth and nineteenth day (Table 2). Statistically significant
negative correlations were found between TXx values and productivity in control plots on days 4, 14
and 19 and in plots with medium thinning on days 1, 7, 14, 15 and 19. In the heavily thinned plots, a
statistically significant positive correlation was detected on the twentieth day (Table 2). Concerning
the parameter TNn, a statistically significant negative correlation with the production of B. edulis was
found only in heavily thinned plots with litter present on the fourth day following the occurrence of
the climatic event.

Discussion

Various studies highlighted the relationship between mushroom production, climatic parameters (e.g.,
Salerni et al., 2002; Alonso Ponce et al., 2011; Martínez-Peña et al., 2012a; Boddy et al., 2014;
Ágreda et al., 2015; Büntegen et al., 2015; Primicia et al., 2016; Andrew et al., 2018; Collado et al.,
2019; García-Bustamante et al., 2021) and silvicultural treatments (Salerni and Perini, 2004; Bonet
et al., 2012; Castaño et al., 2018; Karavani et al., 2018; Sánchez-González et al., 2019; Salerni et al.,
2020). Only in a few cases the production of basidiomata has been related with climatic instability
(Kauserud et al., 2008; Ágreda et al., 2015; Alday et al., 2017) and, as far as we know, it has not been
evaluated whether silvicultural treatments (beyond influencing the production) can also mitigate the
effects of climate instability. The present research, integrating the study carried out by Salerni and
Perini (2004), confirms medium thinning (removal of approximately 20% of the stand basal area) as
the most effective silvicultural treatment to enhance the production of B. edulis, with respect to heavy
thinning (40%) or no thinning. Similarly, Egli and Ayer (1997) showed that the production of edible
mushrooms in mixed forests in Switzerland increased by removing about 35% of the stand basal area,
while more intensive thinning (40–75%) inhibited the production of various edible fungal species
(Pilz et al., 2006; Bonet et al., 2012).




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Table 2 - Significant Pearson correlations between the number of basidiomata of B. edulis observed in each of the 21 days following an extreme climatic event (R20 - days with
intensive precipitation, i.e. ≥ 20 mm; TXx - maxima of daily maximum temperature; TNn - minima of daily minimum temperature) and the climatic values of the same extreme events
throughout the overall study period (2000-2002). Different treatment types (control no thinning, medium thinning, heavy thinning, with litter present or absent) were also considered.

day       Control-no thinning                                       Medium thinning                                         Heavy thinning
          Litter present               Litter absent                Litter present              Litter absent               Litter present                Litter absent
          R20       TXx     TNn        R20       TXx        TNn     R20        TXx    TNn       R20      TXx    TNn         R20        TXx      TNn       R20       TXx   TNn
 1                                                                             -,397*                    -,431*
 2                                                                  ,612*
 3
 4                   -,381*                                                                               -,397*                                -,720*
 5                                                                                                        -,372*
 6
 7                                                                            -,389*                      -,384*
 8
 9
 10
 11
 12        ,623*                                                    ,605*                                                                                 ,593*
 13                                                                                                                         -,716*
 14                  -,395*                                                   -,431*
 15                                                                           -,389*
 16
 17
 18                                                ,634**
 19                  -,413*                                                   -,412*                      -,402*            -,652*
 20                                                ,477*                                                                              ,665**
 21
Statistical significance: * p ≤ 0.005; ** p ≤ 0.001



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    Kavarani et al. (2018) highlighted the link between mushroom production and temperature and
reported that extreme values (minimum and maximum) have greater influence on fruiting processes.
Moreover, according to Andrew et al. (2018), temperature is the most influencing parameter for the
beginning of fruiting, by anticipating or postponing it. These evidences also agree with the results of
our study. Furthermore, the interaction between silvicultural treatments (thinning and litter removal)
and climatic parameters highlighted the role of rain on the production of B. edulis, especially after
the tenth day following a high intensity phenomenon (R20 ≥ 20 mm). This timing was already
noticed by Salerni et al. (2002) studying the fruiting processes of various fungal communities in the
Mediterranean area, where the greatest number of species fruited just 10 days after the rain. In the
case of B. edulis, the influence of precipitation on fruiting processes seems to be linked both to the
rain recorded in the period preceding the fruiting season (García-Bustamante et al., 2021) and to that
of the production period itself (Parladé et al., 2017).
    As regards the possibility of silviculture to mitigate the effects of climate extremes, our results
showed that sudden increases in maximum temperature (here about 8 °C) compared to the average of
the period seemed to have an inhibitory effect on the productivity of B. edulis in those experimental
plots affected by no treatments (i.e., no-thinning and no litter removal). Such phenomenon was also
noticeable in sites treated by medium thinning (removal of approximately 20% of the stand basal
area) and with litter present, while it appeared attenuated in sites with heavy thinning (removal of
approximately 40% of the stand basal area), where fruiting processes seemed to be favoured by high
temperatures, starting from the twentieth day following the event.
    According to some studies, the removal of herbaceous vegetation, litter, or humus may have positive
effects on species richness of ECM fungi (Baar and Kuyper, 1998; Smit et al., 2003), also in coniferous
forests (Baar and Kuyper, 1993; Baar and Ter Braak, 1996). On the other hand, in general, soil litter
is considered an ecologically relevant part of the terrestrial compartment and its vital importance for
maintaining biological communities and their large biodiversity is highlighted by many other works
(Savoie and Largeteau, 2011 and references therein). In line with this and as also previously observed
by Salerni and Perini (2004), our results show that an intensive litter removal can have negative
effects on the fruiting process of B. edulis. The variable outcomes related to litter removal on ECM
productivity suggest that the interactions between forest management and mushroom ecology and
production is much more complex and need to be better understood (Tomao et al., 2017) also in
relation to climatic variability. Several authors hypothesized an impact on production of mushrooms
linked to global climate change, especially in the Mediterranean area (Kauserud et al., 2012; Boddy et
al., 2014; Büntgen et al., 2015; Ágreda et al., 2015; 2016). This scenario has prompted interest in the
development of methods for cultivating ECM (Savoie and Largeteau, 2011) and since forest practices
can affect the occurrence, productivity, and reproduction of mushrooms, they should also consider the
actual influence and risks associated to climatic variability.
    The results of our survey suggest that mycosilviculture may mitigate the effects of environmental
variability caused by climate change. However, further studies are necessary to verify whether such
indications are related exclusively to local and/or temporal factors, as well as to clarify to which
extent the intricate network of relationships between B. edulis and the surrounding environment will
be affected.

Acknowledgements
To Edoardo Casarosa, Piergiuseppe Montini, Walter Pascucci, Sauro Visconti and all members of the
groups of Castiglion d’Orcia and Radicofani for their collaboration.


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