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Chemical Papers 68 (4) 484–492 (2014)
DOI: 10.2478/s11696-013-0477-7
ORIGINAL PAPER
Mineral constituents of edible parasol mushroom
(Scop. ex Fr.) Sing and soils beneath
its fruiting bodies collected from a rural forest area
Edyta Kuldo, Gra˙zyna Jarzy´nska*, Magdalena Gucia, Jerzy Falandysz
Research Group of Environmental Chemistry, Ecotoxicology and Food Toxicology, Institute of Environmental Sciences
& Public Health, University of Gda´nsk, 18 Sobieskiego, 80 952 Gda´nsk, Poland
Received 12 May 2013; Revised 4 July 2013; Accepted 10 July 2013
Concentrations and interrelationships of twenty elements were studied in parasol mushroom and
in the top layer of soil (0–10 cm) from the area of Kiwity (Poland). K, P, Mg, Ca, and Zn were
found to be the most abundant elements in the mushroom. Higher concentrations of Fe, Mn, Na,
Nioccurredinstipesthenincaps,whileCd,Cr,Cu,Hg,Rbdominatedincaps.Ag,Al,and
Ba concentrations in caps and stipes were similar. Parasol mushroom is efficient in up-take and
separation of Ag, Cd, Cu, Hg, K (in caps, the bioconcentration factor is BCF ≥100), Na, P, Rb (50
<BCF <100), and Mg, Zn (BCF >10) in its fruiting bodies, while Al, Ba, Ca, Co, Cr, Fe, Mn, Sr,
and Pb are eliminated (BCF <1). Parasol mushroom from rural forest area in the north-eastern
region of Poland is of hygienic concern for human health because of toxic mercury and cadmium
content in the edible caps, which are also rich in essential Cu, Fe, and their K, Mn, and Zn content
is also high.
c
2013 Institute of Chemistry, Slovak Academy of Sciences
Keywords: trace elements, food, fungi, wild food, wild mushrooms
Introduction
Fungi in nature are involved in biogeochemical
transformation of metallic elements, metalloids, and
other chemical elements taken-up from surface min-
eral soil and humidifying layers and plant biomass
or decomposing litter in which mycelium develops.
Mushrooms are foods for small animals, game, and
many species are edible to man. Mycorrhizal fungi
can in part support associated symbiotic plants
with minerals absorbed and translocated by their
mycelium, while saprophytic species (biomass decom-
posers) block them entirely from their fruiting bodies
(mushrooms, basidiomes, carpophores, sporophores).
Analytical data on the mineral profile of fungus fruit-
ing bodies can also help to understand their nu-
tritional and physiological needs and characteristics
(Paoletti & G¨unthondt-Georg, 2006).
Mushrooms are valued for their sensory, nutri-
tional, and medical properties as well as their mineral
nutrients composition. They surely do not constitute a
significant portion of the food basket worldwide. Nev-
ertheless, consumption of wild grown, and especially
of cultivated and medical mushrooms has significantly
increased in recent years (Chang, 2006; Falandysz et
al., 2011). Cultivated mushrooms are limited to thirty
species so far while there are at least two thousands
wild grown ones (Chang, 1990, 2006). The intake rates
of wild mushrooms vary between the nations (Zhang
et al., 2010); however, wild and also cultivated mush-
room species are an important ingredient for the local
societies and vegetarians’ meals worldwide.
Wild grown mushrooms can be rich in metals es-
sential or toxic to humans (Falandysz & Borovička,
2013; Li et al., 2013; Szubstarska et al., 2012). Even
species collected from the background (pristine) ar-
eas can be abundant in toxic cadmium or mercury
(Chudzy´nski et al., 2009; Melgar et al., 1998). Chem-
*Corresponding author, e-mail: grazyna.jarzynska@gmail.com
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E. Kuldo et al./Chemical Papers 68 (4) 484–492 (2014) 485
ical elements such as Cu, Zn, As, Cd, Hg, Pb, and
Ni at elevated or high concentrations can be found
in mushrooms collected at roadsides or land con-
taminated due to industrial emissions. Hence, mush-
rooming at contaminated sites can be problematic.
Toxic mercury, cadmium, lead, or silver in popular
species of wild growing mushrooms are well docu-
mented (Borovička et al., 2010; Carvalho et al., 2005;
Cenci et al., 2010; Chudzy´nski et al., 2011; Drbal
et al., 1975; Drewnowska et al., 2012a, 2012b; Fa-
landysz, 2002; Falandysz et al., 1994a, 1994b, 2001,
2002a, 2002b, 2003, 2008a, 2012a, 2012b; Falandysz
& Danisiewicz, 1995; García et al., 2009; Jarzy´nska &
Falandysz, 2011a; Melgar et al., 2009; Stijve, 1992; Sti-
jve & Roschnik, 1974; Zimmermannová et al., 2001).
Although the interest in the biodiversity of mush-
rooms and in their content of metals and metalloids
is high, the knowledge of their bioconcentration po-
tential and multimineral composition is poor. Also,
a credible evaluation of the nutritional value of wild
growing mushrooms has been missing so far. This is
due to the fragmentary knowledge of their composition
due to the very limited information on the bioavail-
ability of their constituents (Falandysz, 2008, 2012;
García et al., 2009).
Mushrooms can bioconcentrate various metal ions
in their fruiting bodies and some can be considered
as hyper-accumulators of certain metals (Borovička et
al., 2010). Principal factors influencing the accumula-
tion of heavy metals in the fruiting bodies are fungal
factors such as the development of mycelium, fungal
structure, biochemical composition, nutritional needs,
substrate decomposition activity, morphological por-
tion; geological and environmental factors such as the
metallic elements, metalloids, and other chemical el-
ements abundance, and availability to mycelium; no
evidence was found on a definite role of soil pH or soil
organic matter content in the accumulation in fruiting
bodies under real conditions (Alonso et al., 2003; Br-
zostowski et al., 2009; Falandysz & Brzostowski, 2007;
García et al., 1998). An experiment showed that in
contaminated aqueous solutions, pH has a decisive role
in the biosorption of metals by Agaricus macrosporus
(Melgar et al., 2007).
Parasol mushroom is one of the most distinctive
members of the Agaricaceae family and it is a sapro-
phytic species. This fairly common mushroom grows
alone or scattered in well-drained soils in pastures
(near lakes and rivers) and at the edge of woods in
temperate climate. Parasol mushroom Macrolepiota
procera (Scop. ex Fr.) Sing, earlier known as Lepiota
procera, is edible. However, no mushroom should be
eaten raw in spite of a common opinion (or tradition
somewhere) on its suitability (caps) as raw (uncooked)
food. This is because not all proteins of mushrooms
and their biological properties are sufficiently known.
A good example is toxic agaritin of Agaricus mush-
rooms that disappears during cooking. The cap of
parasol mushroom has to be cooked before eaten while
stipes are inedible. Beginners in mushrooming should
be very careful with parasol mushroom since it su-
perficially resembles Amanitas. It also has some more
closely related poisonous look-alikes like Chlorophyl-
lum molybdites (Falandysz et al., 2008b; Gumi´nska
& Wojewoda, 1988). This and other species of the
Macropepiota genus take part in biogeochemical cy-
cling of metals, semi-metals, and other mineral ele-
ments absorbed from soils and organic matter for use
by plants, animals, and humans, which is the key role
of many fungi as decomposers in ecosystems (Baptista
et al., 2009; Falandysz et al., 2007, 2008b; Falandysz
& Gucia, 2008; Vetter & Siller, 1997).
Theaimofthepresentworkwastodetermine
the profile and capacity to accumulate mineral con-
stituents in fruiting bodies of parasol mushroom from
a forest and agricultural area in the north–eastern part
of Poland. This region can be considered as unpolluted
and distant from industrial emissions. Also, the con-
tent of some important mineral constituents of mush-
room caps was assessed in view of human nutrition
and toxicological risk.
Experimental
Fifteen mature fruiting bodies of parasol mush-
room were collected from the area of Kiwity (Poland)
in 2003. The site is a typical forest and agricultural
area not subject to direct human activities. Geograph-
ically, the site is situated at the northern edge of the
Olsztyn Lake District in the north–eastern region of
Poland. An unquestionable advantage of the area is
that it is unpolluted by industry. Simultaneously with
mushroom, samples of forest humidifying soil and min-
eral soil layer (0–10 cm), after removing the superficial
layer of litter and organic detritus, were collected at
each stand.
Fresh mushrooms were cleaned from plant and sub-
strate debris with a plastic knife and divided into
two parts; caps and stipes. Each sample was dried
at 65◦
C to constant mass in an electrically heated
laboratory drier. Then, the samples were pulverized
in an agate mortar and kept in polyethylene bags
in dry conditions. Approximately 500 mg of homog-
enized fungal material were weighted to a closed poly-
tetrafluoroethylene (PTFE) vessel and pre-digested
(≈24 h) using 7 mL of a concentrated (65 %) ni-
tric acid solution (Suprapure,Merck,Germany)at
room temperature. The vessels were closed and pres-
sure/temperature digested in an automatic microwave
digestion system MARS 5 (CEM Corporation, USA).
Substrate samples were air dried at room tempera-
ture for several weeks and then sieved through a sifter
(pore size 0.2 mm). The substrate samples (≈2.5 g)
were cold (room temperature) treated with a nitric
acid solution (20 %) in quartz vessels which were kept
open for 24 h. The leachate solutions were filtered us-
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486 E. Kuldo et al./Chemical Papers 68 (4) 484–492 (2014)
ing filter papers (WhatmanNo. 42, GE Healthcare,
Poland) before being diluted to 50 mL with deionized
water (Hydrolab, Poland).
Precision and reproducibility of the method were
determined by analyzing double replicates of the se-
lected samples and calculating the coefficient of vari-
ation, which was lower than 5 % for each element.
Additionally, the methods of elements determination
were validated and controlled by the analysis of several
certified reference material: INST-SRM 1570a spinach
leaves (National Institute of Standard and Technol-
ogy, USA) and CTA-OTL1-oriental tobacco leaves, a
material produced by the Institute of Nuclear Chem-
istry and Technology (Warsaw, Poland), and by an
inter-laboratory calibration trial in this institute (Dy-
bczy´nski et al., 1996).
Concentrations of 20 chemical elements (except
Hg) were determined by inductively coupled plasma
optical emission spectrometry (ICP-OES; Optima
2000 DV, Perkin–Elmer, USA). Determination of the
mercury content was carried out by cold vapor atomic
absorption spectrometry (CV-AAS) using an auto-
mated 3200 Mercury Monitor of the Thermo Separa-
tion Products (USA). Technical and analytical details
of the used methods of chemical elements determina-
tion were described in previous articles (Brzostowski
et al., 2009, 2011a, 2011b; Falandysz, 1990; Falandysz
& Chwir, 1997; Frankowska et al., 2010). Limits of de-
tectionforAg,Al,Ba,Ca,Cd,Co,Cu,Cr,Fe,Hg,K,
Mg, Mn, Na, Ni, P, Pb, Rb, Sr, and Zn were between
0.01–0.10 g per g of dry mass (dm), and 0.005 g
per g of dm for Hg. Coefficients of variation for these
measurements in routine runs were well below 10 %.
The concept of the bioconcentration factor (BCF),
calculated as a quotient between the chemical element
concentration in the caps or stipes and the soil con-
centration, was used to asses the potential of fungus
to accumulate trace elements. A quotient between the
chemical element concentrations in the caps and stipes
(QC/S) was used to express the elements distribution
within the fruiting body of the mushrooms.
Results and discussion
Data on the parameters determined for parasol
mushroom and forest soil substrate are presented in
Tabl e 1.
Concentrations (per g of dm) of the examined
chemical elements occurring in the fruiting bodies of
parasol mushroom in a descending order are as fol-
lows: K (in caps ≈34000) >P(≈12000 g) >Mg
(≈1500 g) >Na (≈300 g) >Cu, Ca, Rb (≈150–
200 g) >Fe (≈100 g) >Al, Zn (≈60–80 g) >Mn
(≈30 g) >Hg, Cd (≈5–7 g) >Ag, Pb, Ba (≈1–
1.5 g) >Sr, Co, Cr (≈0.5 g) >Ni (≈0.01 g)
(Table 1). There are significant (0.05 <p<0.01; U
Mann–Whitney test) differences in the concentrations
of some of these elements in the caps and in the stipes
of parasol mushroom. The caps as compared to the
stipes contain higher concentrations of K, P, Mg, Cu,
Rb, Zn, Hg, Cd, and Sr; median QC/Svalues for these
elements vary between 1.7 and 4.3 (Table 1). Sodium
is present in higher concentrations in stipes than in
caps, while concentrations of Ag, Al, Ba, Ca, Fe, Mn,
and Pb in caps and stipes are similar. These data on
the distribution of elements between caps and stipes,
except those of Pb, Ba, Sr, Cr, and Co, largely agree
with the observations made for a representative collec-
tion of mature specimens of parasol mushroom from
a large and old forest reserve of the Nadwarcia´nskie
Forest in Poland (Falandysz et al., 2008b).
Edible caps of parasol mushroom are rich in potas-
sium with (33000 ±3900) g per g of dm; while the
concentration of sodium is by about 100-fold lower
with (300 ±100) g per g of dm (Table 1). Similarly to
parasol mushroom, many other mushrooms collected
in wild are also a reasonably good source of potassium
such as king bolete (Boletus edulis)with≈30000 g
per g of dm in the caps and larch bolete (Suillus gre-
villei)with≈40000 g per g of dm (Chudzy´nski &
Falandysz 2008; Falandysz et al., 2008a; Frankowska
et al., 2010). Caps of parasol mushroom are also rel-
atively rich in phosphorus ((12000 ±1900) gperg
of dm ) and magnesium ((1500 ±190) gpergofdm).
Concentrations of Cu, Cd, Rb, Fe, Al, and Zn in the
caps are around (100–200) g per g of dm. Some of
these trace metals can be of nutritional importance
due to their abundance in this species (Table 1). Mn
present in the caps of parasol mushrooms is also of
nutritional value but it is usually abundant in many
staple foods and especially in cereals, different animal
meats, and some beverages (beer) (Falandysz, 1991,
1993, 1994; Falandysz et al., 1994c; Jarzy´nska & Fa-
landysz, 2011b; Rose et al., 2010; Wyrzykowska et al.,
2001).
Higher concentrations of Hg and Cd, when con-
sidering their toxicity and importance as possible
food contaminants, were observed in the caps with
(7.4 ±0.5) gpergofdmand(4.7±1.7) gpergof
dm on the average, and maximally with 8.6 gperg
of dm and 7.0 g per g of dm, respectively (Table 1).
Parasol mushroom is known as a species that contains
Hg in its delicious caps even when collected at pris-
tine sites (Falandysz et al., 2007; Falandysz & Gucia,
2008). Cd content in the caps is also relatively high,
which can be explained by the high potential of para-
sol mushroom to take-up and block this element (BCF
= 100). In soil, (0.053 ±0.024) gofCdpergofdm
(Table 1) was found. Cadmium content in the parasol
mushroom caps collected in other regions of Poland is
usually below 2.0 g per g of dm, and in foreign coun-
tries it was up-to around 3-fold higher (Falandysz et
al., 2008b).
Pb and Ag are two other metals harmful to an-
imal body cells. Their concentration in the caps is
<2.0 g of each per g of dm on the average. Pb is more
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E. Kuldo et al./Chemical Papers 68 (4) 484–492 (2014) 487
Tabl e 1 . Mineral content of parasol mushroom and substrate ( gpergofdrymass,mean±SD range (in brackets), and median
values (third line)) from the Kiwity village site, caps to stipes concentration quotient (QC/S), and bioconcentration factor
(BCF) values
Element Cap per g
of dm/ g
Stipe per g
of dm/ g
QC/SSoil per g
of dm/ g
BCFCBCFS
K 33000 ±3900
(25000–42000)
34000
18000 ±47000
(10000–27000)
17000
1.9 ±0.4
(1.1–2.5)
2.0
140 ±49
(96–200)
110
260 ±84
(140–370)
300
140 ±39
(64–190)
140
P 12000 ±1900
(8700–16000)
12000
6400 ±1000
(4100–7500)
7100
1.9 ±0.3
(1.4–2.7)
1.7
220 ±36
(190–275)
220
53 ±8
(40–66)
57
29 ±7
(18–40)
31
Mg 1500 ±190
(1200–1900)
1500
820 ±130
(520–970)
820
1.9 ±0.3
(1.5–2.5)
1.9
200 ±98
(120–350)
140
9.2 ±3.6
(3.8–14.0)
11
4.9 ±1.9
(1.7–7.4)
5.8
Na 300 ±110
(89–530)
300
610 ±240
(230–990)
560
0.52 ±0.17
(0.24–0.87)
0.45
6.2 ±1.2
(4.9–7.7)
6.3
50 ±19
(12–79)
50
100 ±45
(30–180)
110
Cu 180 ±41
(87–250)
190
91 ±17
(51–120)
95
2.0 ±0.2
(1.7–2.4)
2.0
0.74 ±0.23
(0.48–1.10)
0.66
270 ±110
(130–480)
250
130 ±46
(66–220)
120
Ca 160 ±72
(74–300)
130
170 ±80
(93–380)
150
1.1 ±0.5
(0.31–1.70)
0.96
340 ±230
(140–660)
210
0.69 ±0.48
(0.15–1.60)
0.68
0.62 ±0.31
(0.16–1.40)
0.68
Rb 150 ±50
(63–230)
160
50 ±15
(20–70)
52
3.1 ±0.8
(1.5–4.8)
3.1
2.6 ±0.7
(2.0–3.6)
2.2
65 ±28
(18–110)
71
21 ±8
(6–34)
23
Fe 110 ±50
(45–240)
100
120 ±70
(74–300)
93
0.97 ±0.42
(0.43–1.90)
0.91
1900 ±210
(1800–2300)
1900
0.056 ±0.027
(0.023–0.130)
0.052
0.064 ±0.036
(0.032–0.160)
0.050
Al 92 ±71
(31–280)
58
77 ±60
(32–190)
50
1.4 ±0.7
(0.4–2.8)
1.1
1200 ±290
(990–1700)
1100
0.079 ±0.068
(0.021–0.260)
0.051
0.063 ±0.048
(0.020–0.180)
0.044
Zn 83 ±15
(50–110)
81
52 ±9
(38–66)
54
1.6 ±0.3
(1.2–2.3)
1.7
7.7 ±1.5
(6.0–9.3)
7.2
11 ±3
(7–18)
10
7.0 ±1.8
(4.1–9.6)
7.1
Mn 37 ±19
(15–84)
28
48 ±21
(22–87)
45
0.81 ±0.31
(0.48–1.60)
0.72
240 ±185
(57–520)
260
0.28 ±0.25
(0.05–0.83)
0.19
0.37 ±0.36
(0.09–1.40)
0.28
Hg 7.4 ±0.4
(6.3–8.6)
7.4
2.7 ±0.9
(1.2–4.6)
2.7
3.2 ±1.4
(1.7–6.2)
2.7
0.053 ±0.004
(0.048–0.059)
0.053
140 ±14
(126–170)
140
52 ±20
(21–96)
51
Cd 4.7 ±1.7
(1.8–7.0)
4.7
1.9 ±0.9
(0.5–3.1)
1.9
2.6 ±0.6
(1.9–4.2)
2.4
0.053 ±0.024
(0.034–0.089)
0.039
100 ±57
(37–190)
100
45 ±29
(12–83)
45
Ag 1.7 ±0.6
(0.7–3.1)
1.6
2.4 ±0.9
(0.8–4.5)
2.0
0.74 ±0.17
(0.44–1.10)
0.72
0.022 ±0.019
(0.003–0.051)
0.023
190 ±200
(23–650)
92
250 ±240
(33–680)
130
Pb 1.3 ±0.4
(0.7–2.3)
1.2
1.7 ±0.4
(1.2–2.4)
1.6
0.78 ±0.34
(0.48–1.50)
0.66
11 ±1
(10–11)
11
0.12 ±0.04
(0.06–0.21)
0.12
0.16 ±0.04
(0.12–0.23)
0.14
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488 E. Kuldo et al./Chemical Papers 68 (4) 484–492 (2014)
Tabl e 1 . (continued)
Element Cap per g
of dm/ g
Stipe per g
of dm/ g
QC/SSoil per g
of dm/ g
BCFCBCFS
Ba 1.4 ±0.7
(0.8–2.9)
1.1
1.2 ±0.6
(0.6–2.3)
1.1
1.3 ±0.5
(0.7–2.4)
1.3
13 ±5
(8–20)
10
0.12 ±0.07
(0.04–0.28)
0.11
0.10 ±0.06
(0.03–0.22)
0.081
Sr 0.68 ±0.37
(0.06–1.20)
0.66
0.19 ±0.13
(0.06–0.48)
0.14
4.4 ±3.5
(0.3–14)
4.3
1.5 ±1.0
(0.6–3.0)
0.92
0.71 ±0.47
(0.02–1.20)
0.96
0.17 ±0.12
(0.019–0.52)
0.16
Co 0.38 ±0.21
(0.06–0.70)
0.39
ND ND 0.50 ±0.23
(0.29–0.82)
0.42
0.98 ±0.76
(0.13–2.40)
0.79
ND
Cr 0.32 ±0.19
(0.01–0.66)
0.38
<0.01 ND 1.5 ±0.3
(1.3–2.1)
1.4
0.24 ±0.15
(<0.01–0.53)
0.27
ND
Ni 0.015 ±0.029
(0.010–0.110)
0.01
ND ND 0.99 ±0.48
(0.65–1.70)
0.68
0.022 ±0.046
(<0.01–0.17)
0.007
ND
BCFc – Bioconcentration factor in caps; BCFs – bioconcentration factor in stipes; ND – not determined.
abundant but fairly less bioavailable in this species
compared to the very efficiently bioconcentrated Ag
(Table 1). For example, at a high-traffic road-side in
Portugal, this mushroom contains (29 ±2) gofPb
per g of dm, while a ten-fold lower concentration was
found at the reference site. Also Cur in the vineyards
of different age and polluted by copper pesticides ac-
cumulates in parasol mushroom depending on the Cu
concentration in soil (Carvalho et al., 2005).
Information about the concentration of Ba and Sr
in parasol mushroom is limited. In this study, the
mean value of the Ba content in the caps did not ex-
ceed 1.5 gpergofdmandthemedianwas1.1 g
per g of dm; for Sr, the mean and the median were
0.68 gpergofdmand0.66 g per g of dm, respec-
tively (Table 1). Ba and Sr are in the second group of
the periodic table, and in mushrooms there is an ac-
curate linear relation (p<0.05) between the contents
of these two metals (Falandysz et al., 2008b). Pat-
terns of Ba and Sr accumulation in caps and stipes
differ and Ba in stipes is much more abundant then
Sr. Vetter and Siller (1997) determined 2 gofBa
per g of dm in young and 4 gofBapergofdmin
mature (old) fruiting bodies of parasol mushroom in
Hungary. In a study in Poland, Ba in caps did not
exceed 1.5 g per g of dm on the average, while in
stipes it was 8.5 gofBapergofdmand9.3 g
of Ba per g of dm (two specimens), which is approxi-
nately 50-fold higher than in the caps; also the content
of Sr in the stipes was high, i.e. 3.1 gpergofdm
and 3.5 g per g of dm (Falandysz et al., 2008b).
Parasol mushrooms at the site surveyed were poor
in Ni and relatively more abundant in Co and Cr,
the mean values were 0.015 gpergofdm,0.38 g
per g of dm, and 0.32 g per g of dm, respectively
(Table 1).
The caps of parasol mushroom fried fresh, with
eggs or alone, are very tasty and highly valued by
fanciers. However, this spectacular mushroom, due to
a specific habitat, fragility of caps, and high competi-
tion between the mushroomers is eaten only by a few
in Poland. Hence, if hunted in the area of Kiwity, it
can become an ingredient of a single meal (300–500 g
– a big portion in summer time), in which the intake
of between 222 g and 370 g of Hg, 140 gto235 g
of Cd, 51 gto85 g Ag, and 36 gto60 gofPb
(median values for a 300 g and 500 g mushroom meal;
water content of 90 %; no loss of metals during cook-
ing). These intakes correspond to doses of 3.7 gto
6.1 gofHgperkgofbodymass(bm;60kgbmper-
son), 2.3 gto3.9 gofCdperkgofbm,0.85 gto
1.4 g of Ag per kg of bm, and 0.6 gto1.0 gofPb
per kg of bm.
For Hg, the reference dose (RfD) is 0.3 gperkg
of bm daily (US Environmental Protection Agency)
and the value of tolerable daily intake rate of 0.61 g
per kg of bm (0.23 g methylmercury) is derived from
the Provisionally Tolerable Weekly Intake (PTWI)
of 4.3 g per kg of bm or 260 g for an individual
of 60 kg of bm by Food and Agricultural Organi-
zation and World Health Organization (FAO/WHO)
(JECFA, 1978, 2007; Schultz & Breidenbach, 1987).
In light of these limits, one meal made of 300–500 g
of parasol mushroom caps from the site surveyed can
be considered safe. It is possible that some fanciers of
this species can eat its caps several times in a week
in a mushrooming season (assuming its availability
in northern Poland from July to August; in warmer
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E. Kuldo et al./Chemical Papers 68 (4) 484–492 (2014) 489
regions of Europe from June to September), which
results in exceeding the given hygienic limits. Nev-
ertheless, bioavailability of inorganic Hg from caps of
parasol mushroom (also methylmercury) to humans is
not known.
For Cd and Pb, doses of 1 gofCdperkgofbm
daily and 3.6 g of Pb per kg of bm daily are tolerable
intake rates derived from PTWIs (420 gofCdand
1500 g of Pb weekly for a 60 kg person) recommended
by the Joint FAO/WHO Expert Committee on Food
Additives (WHO, 1989, 1993). Certainly, a 300–500 g
meal of parasol mushroom eaten once in a week pro-
vides Cd in a relatively large single dose exceeding the
hygienic limits by 2.3 to 3.9-fold. For Pb, these figures
are from 3.6 to 6.0-fold below the limit. Hence, caps of
parasol mushroom are an important source not only
of Hg but also of Cd. Bioavailability rates of Cd and
Pb from meals containing caps of parasol mushroom
are unknown. Caps of parasol mushroom can be con-
sidered as a good dietary source of Cu, Fe, and K and
a valuable one of Mn, Se, or Zn. Data on the rates of
this mushroom intake in Poland or elsewhere are not
reported.
BCF provides an insight into a species potential
(Table 1) of up-take and blockage of mineral con-
stituents in its fruiting bodies. Parasol mushroom is
efficient in the bioconcentration of Ag, Cd, Cu, Hg, K
(median BCF ≥100), Na, P, Rb (50 <BCF <100),
and Mg, Zn (BCF >10), and the blockage of Al, Ba,
Ca, Co, Cr, Fe, Mn, Sr, Pb (BCF <1) in its fruiting
bodies.
Alonso et al. (2003) found that saprophytes, such
as parasol mushroom and white bottom mushroom
(Agaricus bisporus), have lower BCF values for Cu
and Zn compared to the mycorrhizal species such as
king bolete (Boletus edulis), safron-milk cap (Lactar-
ius deliciosus), and brown birch scaber stalk (Lec-
cinum scabrum). In our earlier studies, king bolete
efficiently bioconcentrated Cd, Cu, Hg, K, Mg, and
Zn (BCF >1) and, with an exception of Hg, its ef-
ficiency for Cu and K was lower compared to that of
parasol mushroom (Table 1) (Falandysz et al., 2007,
2011).
Parasol mushroom plays an important role in the
biochemical transformation of chemical elements. Our
results show that the capacity of this species to accu-
mulate minerals such as Ag, Al, Ba, Ca, Cd, Co, Cu,
Cr,Fe,Hg,K,Mg,Mn,Na,P,Pb,Rb,Sr,andZn
abundant or poor in soil in its fruiting bodies is high.
For the principal component analysis (PCA), data
were adjusted to a normal distribution using the Box–
Cox transformation. The analysis was based on the
correlation matrix and the reference significance level
of p<0.05. PCA data revealed that 97 % of infor-
mation regarding the minerals (18 elements) composi-
tion variability of parasol mushroom and soil from the
rural forest area can be described by three principal
components (PCs) (Figs. 1 and 2). The varimax rota-
Fig. 1. Plot of loadings (varimax rotation) based on the con-
centration of elements in caps and stipes of parasol
mushroom and forest soil substrate considering the first
and second factors.
Fig. 2. Plot of loadings (varimax rotation) based on the con-
centration of elements in caps and stipes of parasol
mushroom and forest soil substrate considering the first
and third factors.
tion method helped with data interpretation and led
to the conclusion that cases vary rather due to sev-
eral interacting elements than due to the particular
element content. The first factor (eigenvalue = 12.4)
explains approximately 69 % of the total variance and
consists of positively correlated K, P, Mg, Cu, Rb, Zn,
Hg, and Cd. This factor indicates the presence of in-
dustrial or pesticide pollution; however, as mentioned
earlier, parasol mushroom is known as a species con-
taining elevated concentrations of Hg in its fruiting
bodies even when collected in pristine sites. The sec-
ond component (eigenvalue = 3.7), formed primarily
by negatively correlated Ca, Fe, Al, Mn, Pb, Ba, Sr,
and Cr, accounts for 21 % of the total variance. The
source of the components of this factor is the contri-
bution mainly from traffic. Factor three (eigenvalue
= 1.3) is positively correlated with Na and Ag with
a medium loading value (0.91 and 0.84, respectively)
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490 E. Kuldo et al./Chemical Papers 68 (4) 484–492 (2014)
and explains 7.3 % of the total variance. The source
of this factor is probably soil. Figs. 1 and 2 show the
relationship between metals in the factor space. For
example, Pb–Fe, Al–Ba, and Cr–Mn cluster together
(associated with PC2). Trace elements such as K–P–
Mg–Cu–Hg–Zn and Cd–Rb tend to cluster together
when associated with PC1. Pairs of Na and Ag, as-
sociated with PC3, are separated from other metals
(Figs. 1 and 2). Other metals are not apparently asso-
ciated with a definite-factor axis. This configuration
of cluster intercorrelations can be explained by the
dependence of the macro and trace metals concentra-
tions in higher mushrooms on several factors, includ-
ing biological ones (Falandysz et al., 2008b).
Conclusions
The results of this survey indicate that caps of
parasol mushroom from the rural forest areas in the
north–eastern region of Poland can be of hygienic con-
cern. This is because of their higher Hg and Cd con-
tent, while this species is also rich in essential Cu,
Fe, and K and its content of Mn, Se, or Zn is also
high. Because of the high bioconcentration potential
of parasol mushroom for Ag, Cd, Cu, Hg, K, Na, P,
Rb, Mg, and Zn and a relative abundance of Al, Ba,
Ca,Co,Cr,Fe,Mn,Sr,andPbinthesoil,fruiting
bodies of this species are rich in many metals as well
as in P, which increases the role of this species in the
biogeochemical transformation of mineral constituents
of soil in animals and men.
Acknowledgements. This study was funded by the Na-
tional Science Centre on basis of the decision No. UMO-
2011/03/N/NZ9/04136.
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