Heavy Metals in Edible Wild-Growing Mushrooms in Norway
Trond Magne
Storstad[1],
Eiliv Steinnes1, and Bjørn Ove Berthelsen[2]
ABSTRACT
Uptake of Cu, Zn, Cd and Pb by
the naturally occurring mushroom species Albatrellus
ovinus, Boletus edulis, Cantharellus cibarius, Hydnum repandum and Leccinum versipelle was studied in
regions with high (Southern Norway) and low (Central Norway) concentrations of
these metals in surface soils. Metal concentrations in fungi were appreciably
higher in Southern Norway. B. edulis and L. versipelle accumulated cadmium to levels that might represent a
health risk to mushroom consumers. The lowest bioconcentration by fungi was
observed with respect to lead. Ammonium nitrate or oxalate extractable metal
fractions in organic surface soils can hardly explain metal uptake by the fungi
studied.
INTRODUCTION
Natural ecosystems in
southernmost parts of Norway are strongly polluted by heavy metals due to
long-range atmospheric transport from other parts of Europe. Among these are
cadmium, lead and zinc (Steinnes et al.
1997). The long-term atmospheric deposition has led to a strong enrichment of
these metals in organic surface soils (Steinnes et al. 1989). In contrast, the central parts of Norway are
considerably less polluted.
Several species of macrofungi
are known to accumulate certain heavy metals to concentrations often one or two
orders of magnitude higher than most plant species, also from soils with rather
low concentrations, even though a large species variability is often observed (Tyler,
1980; Lepp, 1992; Berthelsen et al., 1995).
Knowledge of metal concentrations in edible mushrooms may therefore be of
toxicological importance. The main objectives of this project are to compare
the concentrations of heavy metals in fungi and soils, and to assess possible
health risks to the consumers of these fungi.
METHODS
Altogether, about 200 samples
of five edible mushroom species were collected from 19 spruce forest sites in
southernmost Norway (Aust-Agder county) and from 13 sites in central Norway
(Trøndelag counties), autumn 1997. For each species, about 20 samples were
collected from each of the two areas. The species are Albatrellus ovinus, Boletus edulis (Penny Bun), Cantharellus cibarius (Chanterelle), Hydnum repandum (Hedgehog Fungus) and Leccinum versipelle (Orange Birch Bolete). These are all
ectomycorrhizal fungi, and are among the most commonly consumed mushrooms in
Norway. For each mushroom sample a corresponding sample of organic surface soil
was collected, just beneath the fruitbody. Mushroom and soil samples were
analyzed with respect to Cu, Zn, Cd and Pb by flame and graphite furnace AAS
after digestion with concentrated nitric acid. A selection of the soil samples
were subject to extractions with 0.05 M and 0.2 M oxalate buffer (pH 4) and 1 M
ammonium nitrate, to examine whether these metal fractions could explain the
observed uptake by mushrooms.
RESULTS AND DISCUSSION
Nitric acid extractable
concentrations of Cu, Zn, Pb and Cd in mushroom and soil samples are shown in
Figure 1. Considerable species and area differences are evident for most of the
metals. A. ovinus and H. repandum have low levels of all the
metals, whereas L. versipelle and B. edulis have higher concentrations in
general. Metal concentrations, except Cu, in both soil and fungi are
considerably higher in the southern area. Species differences with respect to
accumulation of heavy metals are also expressed by fungus/soil concentration
ratios in Table 1. Ranges of bioconcentration factors are less different between
the two areas than metal concentrations in fungi.
Lead concentrations in
mushrooms are low compared to the levels in surface soil (median and maximum Pb
concentrations in soil are 110 and 500 mg/kg in south Norway, and 19 and 48
mg/kg in central Norway, respectively). This is probably because the strong
affinity of Pb for organic matter strongly reduces its bioavailability.
Two species (B. edulis and L. versipelle) show a strong accumulation of Cd, up to 20 mg/kg, or
up to 77 times the concentration in the surface soil.
The Joint FAO/WHO Expert
Committee on Food Additives and Food Contaminants have recommended a
provisional tolerable weekly intake (PTWI) of 400-500 mg Cd and 1,75 mg Pb for an adult of 70 kg (WHO/FAO 1989; WHO/FAO 1993).
Estimated total daily intake for adults in non-polluted areas is 10-40 mg Cd and 15-30 mg Pb. If, hypothetically, the most contaminated mushrooms from the
present study (B. edulis or L. versipelle) were added to this
intake, the required amount to exceed the PTWI of cadmium would be about 6 g
dried mushroom, or about 70 g fresh mushroom per week. For Pb, the required
amount to exceed the PTWI would be about 160-200 g dried mushroom, or about 2
kg fresh mushroom per week. Cd in mushrooms is thus a possible health problem for
consumers, whereas Pb is not.
Oxalate and ammonium nitrate
extractable Cu and Zn concentrations in the soil samples corresponded poorly
with the concentrations found in the mushrooms. Such extractions are therefore
not suitable for predicting Cu or Zn concentrations in the fungal species
studied in the present project.
REFERENCES
Berthelsen BO, Olsen RA,
Steinnes E (1995), Sci. Tot. Environ. 170: 141-149
Lepp NW (1992), In: Uptake and
Accumulation of Metals in Bacteria and Fungi (DC Adriano, Editor), Boca Raton,
Lewis Publishers, pp. 277-298
Steinnes E, Solberg W,
Petersen HM, Wren CD (1989), Water, Air, Soil Pollut. 45:207-218
Steinnes E, Berg T, Vadset M,
Røyset O (1997), Report 691/97, Norwegian State Pollution Control Authority,
Oslo
Tyler G (1980), Trans. Br.
Mycol. Soc. 74: 41-49
WHO/FAO (1989), WHO Technical
Report Series 776, Geneva
WHO/FAO (1993), WHO Technical
Report Series 837, Geneva
Figure 1. Metal
concentrations in the investigated mushrooms and in organic surface soil samples.
Boxes represent the 25-percentile, median and 75-percentile values. Outliers
and extremes (values more than 1.5 or 3 box-lengths from the 75-percentile) are
shown with circles and asterisks, respectively. Vertical lines represent the
range of values that are not outliers or extremes.
Table 1. Ranges
of bioconcentration factors, BCF (conc. in mushroom/conc. in soil) for the
species studied. Values for South and Central Norway are shown together.
|
Species |
BCF Cu |
BCF Zn |
BCF Cd |
BCF Pb |
A.ovinus |
0.04 - 2.0 |
0.37 - 2.9 |
0.45 - 15 |
0.0013 - 0.0093 |
|
C.cibarius |
2.2 - 9.6 |
0.49 - 8.7 |
0.22 - 7.9 |
0.0041 - 0.042 |
|
H.repandum |
0.50 - 5.7 |
0.41 - 4.8 |
0.23 - 9.3 |
0.0041 - 0.029 |
|
L.versipelle |
1.1 - 14 |
1.2 - 8.2 |
0.65 - 77 |
0.00028 - 0.48 |
|
B.edulis |
0.76 - 7.9 |
1.2 - 7.5 |
2.2 - 37 |
0.00090 - 0.32 |