Open Journal of Air Pollution, 2013, 2, 56-62 Published Online September 2013 (
Effect of Mulching on Uptake of Copper and Nickel from
Smelter-Polluted-Soil by Planted Tree Seedlings
Eva Komanicka1,2, Heljä-Sisko Helmisaari3, Markus Hartman2, Tiina M. Nieminen2
1Department of Geochemistry, Faculty of Natural Sciences, Comenius University Bratislava, Bratislava, Slovakia
2Finnish Forest Research Institute, Metla, Vantaa, Finland
3Department of Forest Sciences, University of Helsinki, Helsinki, Finland
Received June 5, 2013; revised July 22, 2013; accepted August 2, 2013
Copyright © 2013 Eva Komanicka et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Our aim was to determine the long-term effect of a mulching treatment on copper (Cu) and nickel (Ni) uptake by tree
seedlings (Pinus sylvestris L. and Betula pubescens Ehrh.) from smelter-polluted forest soil in southwestern Finland. A
mulch cover spread onto polluted barren soil did not have a clear positive impact on the biomass production and it did
not decrease metal uptake by planted tree seedlings during a ten-year study period. In contrast, the Cu uptake by the
above-ground parts of birch was increased as a result of mulching, although there were weak indications of slightly re-
duced availability of Cu and Ni to roots in the case of both species. As Cu and Ni concentrations of foliage and bark
have been shown to be strongly affected by surface deposited metal containing aerosols, only the woody compartments
were used as indicators of metal uptake from soil. The Cu:Ni ratios of woody compartments were lower than those pre-
dicted by the Cu:Ni ratios of soil suggesting that the soil extraction method used gives an underestimation of available
Ni in relation to Cu. The lower soil Niexch concentrations on the mulched plots compared to the controls were in agree-
ment with the slightly lower root Ni concentrations in the mulch treatments.
Keywords: Bioavailability; Biocompost; Birch; Forest Soil; Pine; Restoration; Wood Chips
1. Introduction
Several methods have been developed to ameliorate site
conditions and enhance plant establishment and growth
on metal contaminated environments. Different remedia-
tion agents, such as lime and fertilizers [1], compost and
beringite mixture [2] and application of mulch [3-6] have
been used in environmental restoration approaches. In
addition to providing nutrients into soil, the high organic
matter content of biowaste composts improves the water-
holding capacity, cation exchange capacity and nutrient
availability of soil, which in turn improve tree growth
Plants reveal different patterns in the uptake of trace
elements [8,9]. The vascular plants take up elements
mainly by their roots from the soil, even if the foliar up-
take of gases and soluble elements may also take place
[10]. Trees have been suggested as a low-cost, sustain-
able and ecologically sound solution to the remediation
of heavy metal-contaminated land [11]. Benefits arise
mainly from stabilization of the soil, but in many cases,
trees may be sufficient to provide clean-up of the soil.
Before the beneficial effects can be obtained, the trees
must become established on a site [12]. However, on
highly contaminated soils, tree establishment may be
inhibited by metal toxicity. In less contaminated soils,
other factors may limit plant growth, such as macronu-
trient deficiencies [13] and physical conditions, espe-
cially those properties leading to poor water holding,
aeration and root penetration [14].
The effects of mulching have been reported to vary
greatly according to site, plant species and mulch types
[15,16]. However, only few studies on long-term effects
of mulching on plant metal uptake have been reported. It
is known from an earlier paper based on our study fields
that mulching favored establishment of transplants and
enhanced natural recolonization by pioneer species [17].
The aim of this paper was to assess the long-term effect
of mulching on biomass production and Cu and Ni up-
take by seedlings of pine (Pinus sylvestris L.) and birch
(Betula pubescens Ehrh.) grown for a ten-year-period on
a metal-contaminated site.
opyright © 2013 SciRes. OJAP
2. Methodology
2.1. Study Site
The study site at Harjavalta (61˚19'N, 22˚9'E), south-
western Finland has been subjected to a heavy pollution
load from a large metallurgical complex for several dec-
ades. Smelting of copper started in the area in 1945 by
Outokumpu Oy, while the nickel smelter and refinery
were established in 1959. The surrounding heathland Scots
pine forests are suffering from severe needle loss and
growth retardation [18,19] and high fine root mortality
[20]. The understory vegetation is almost completely de-
graded [21,22] and even though viable seeds have been
found in the forest soil close to the smelters, no seedling
rooting takes place [23].
The long term (1960-1990) mean annual temperature
at a nearby weather station of the Finnish Meteorological
Institute is +4.0˚C and the annual precipitation 558 mm.
The mean annual temperature and annual precipitation
during the study period (1996-2005) were 5.3˚C ± 0.6˚C
and 591 mm ± 62 mm, respectively. The metallurgical
plants are located on a forested esker running in a NW-
SE direction. The soil consists of sorted fine or sorted
fine/coarse sand with no stones. The soil was classified
as an orthic Podzol [24]. The uppermost part of the forest
floor consists of a dark thick layer of undecomposed lit-
ter, as a result of strongly retarded microbial activity and
impaired mineralization [25].
2.2. Remediation Experiment
In June 1996, tree seedlings were planted at a distance of
ca. 500 meters from the main stack of the Cu-Ni smelters.
Seedlings of two native species, Betula pubescens Ehrh.
(1-year-old containerized downy birch seedlings) and
Pinus sylvestris L. (2-year-old containerized Scots pine
seedlings), were each planted on six replicate plots (5 × 5
m2) as 49 seedlings per plot. Three of the plots were to-
tally covered with a 5 cm-thick layer of mulch, and the
other three were left uncovered to serve as controls. In
addition, six replicate plots (5 × 5 m2) without any trans-
plants were established to serve as reference sites for soil
characteristics. Three of them were covered with a 5
cm-thick layer of mulch, and the other three were left
uncovered. The location of the experimental plots was
randomized. One of the uncovered plots was uninten-
tionally destroyed when slag was spread over it.
The pine and birch seedlings were planted in soil
pockets (2 L, depth about 20 cm) containing mulch.
Planting the seedlings in the mulch pockets penetrating
down into the less contaminated soil was considered to
be essential for their initial survival [17].
The mulch consisted of a mixture of household bio-
compost and woodchips (1:1, volume). The biocompost
was 14 months old and had been produced in outdoor
windrows at the Ämmässuo Waste Handling Centre,
Espoo, Finland by mixing kitchen and garden waste from
the Greater Helsinki area and coarse woodchips (diame-
ter ca. 50 mm). The mulch was prepared one week before
spreading by mixing the biocompost with woodchips
(diameter < 20 mm) of Scots pine and Norway spruce
(Picea abies Karst.) stemwood [26]. The pH of the mulch
was 6.3 and the carbon:nitrogen ratio 16:1 [26]. The av-
erage Cu and Ni concentrations in the Ämmässuo bio-
compost were 60 and 3 mg·kg1 as dry weight [26]. The
mulch was spread directly on the layer of undecomposed
litter with a plotwise dose of biocompost (excluding the
woodchips) of 5.4 kg·m2 as dry weight. The input of C
through mulching was 2 kg·m2 [26].
2.3. Harvest of the Seedlings and Soil Sampling
After a 10 year period, 3 seedlings from each experi-
mental plot (3 replicate plots for both control and mul-
ching) were harvested in August 2005. One of the seed-
lings was chosen among the tallest individuals, the sec-
ond to represent the smallest ones, and finally the third
one to represent the medium size. After removing the
foliage, the youngest shoots (formed in 2005) and all
roots were separated from the seedlings, and bark was
carefully peeled away from the remaining part to obtain 5
compartments: foliage, young shoots, bark, wood, roots.
The pine needles were grouped according to the year of
their formation: Current, current + 1 year, current +2 and
current +3 + older needles.
The soil samples were collected with an auger (diame-
ter 58 mm) at the same time as seedlings were harvested.
Three cores per plot were taken and after removing the
organic layer the mineral soil was divided in layers of
5-cm-thickness (0 - 5, 5 - 10, 10 - 15, 15 - 20, 20 - 25,
and 25 - 30 cm).
2.4. Analytical Methods
The plant samples were dried and weighed. After weigh-
ing the three replicates of each compartment from each
plot were bulked together to give one composite sample
of each compartment per plot, thus resulting in three rep-
licate composite samples per treatment. The organic
layer samples of the soil cores were dried and milled to
pass through a 1 mm sieve, and thereafter they were di-
vided into two parts for the total and exchangeable ana-
lysis. Total Cu and Ni concentrations from the organic
soil and plant samples were determined, following mi-
crowave assisted wet digestion in HNO3 and H2O2, by
Inductively Coupled Plasma Atomic Emission Spec-
trometry (ICP-AES).
Exchangeable Cu and Ni were determined by extrac-
tion with 0.1 M BaCl2 + 2% EDTA, (7.5 g of mulch or
15 g of mineral soil/150 ml extractant, shaking for 2
Copyright © 2013 SciRes. OJAP
hours) followed by filtration and analysis by ICP-AES.
2.5. Statistical Analyses
We used the two way t-test to study the effect of the
treatment on biomass and metal concentrations and the
between-species variation.
3. Results
3.1. Biomass Production
There were no statistically significant differences in bio-
mass production during the ten-year period between the
mulch and control treatments, although the mean bio-
masses of both pine and birch tended to be slightly
higher on the mulched plots (Figure 1).
3.2. Metal Concentrations
3.2.1. Foliage
The Cu and Ni concentrations of pine needles tended to
increase with age but no statistically significant differ-
ences could be found between the treatments (Table 1).
In case of birch the Cu and Ni concentrations of the
leaves were slightly higher in the mulch treatment, but
the differences were not statistically significant (Table
3.2.2. Bark
The highest Cu and Ni concentrations of all the sampled
compartments were those of pine bark from the control
plots (Figure 2). The t-test showed that the between-
treatment difference was statistically significant for the
Cu concentrations (t = 4.039; p = 0.016).
The mean Cu concentration of the birch bark was
slightly higher on the mulch plots, but the difference was
not statistically significant. The corresponding Ni con-
Figure 1. Mean total biomass of the sampled tree seedlings
by treatments, n = 9 for both species. The bar indicates the
Table 1. Mean (± standard
standard error of the mean.
error of the mean) Cu and Ni
Copper Nickel (mg·kg1)
concentrations of pine needles by needle age classes (C =
current needles, C + 1 one-year-old needles, C + 2 two-year-
old needles and C + 3 three-year-old needles), n = 3 in
Pine needle
ContrMlch ControlMulch
age class
ol u
mean323 237 71.1 61.0
C + 3
C + 2
C + 1
Mn467 712 127 156
st err±133 ±24.0 ±27.5 ±6.95
mean435 393 73.7 78.23
st err±70.4 ±76.3 ±9.02 ±8.49
mean292 325 66.6 76.03
st err±19.1 ±68.9 ±5.15 ±10.19
mean116 124 46.0 42.3
st err±3.18 ±18.0 ±1.54 ±2.90
St err64.6 104 23.0 14.7
Figure 2. Mean Cu and Ni concentrations in barine
entrations were about the same for both treatments (Fi-
3.2.3. Above Grou nd W oody Comp a rt ments and
The Ci concentrations of the youngest shoots
k of p
and birch by treatments, n = 3. The bar indicates the stan-
dard error of the mean.
gure 2).
u and N
were much lower than those of bark, but there were no
statistically significant differences between the treat-
ments (Figure 3). The Cu and Ni concentrations in pine
wood appeared to be slightly higher on the control plots,
but the differences were not statistically significant (Fi-
Copyright © 2013 SciRes. OJAP
gure 4).
The mean Cu and Ni concentrations in both pine and
3.2.4. Soi l Concentrations
in the mineral soil layers
rch roots were slightly higher on the control plots com-
pared to the mulch treatment, but the differences were
not statistically significant (Figure 5).
The Niexch concentrations
tended to be lower in the mulched plots compared to the
control, while the differences between the treatments in
the Cuexch concentrations of the mineral soil were small
(Figure 6). The Niexch concentrations were much lower
than the Cuexch concentrations, roughly ten times lower.
Figure 3. Mean Cu and Ni concentrations in the youngest
shoots of pine and birch by treatments, n = 3. The bar
indicates the standard error of the mean.
Figure 4. Mean Cu and Ni concentrations in wood (ithout
indicates the standard error of the mean.
bark) of pine and birch by treatments, n = 3. The bar
4. Discussion
duction and Metal Uptake 4.1. Biomass Pro
Both Scots pine and downy birch are considered as m
tolerant species, since they are able to survive in metal-
polluted areas around smelters [17,27-29]. Restricted
uptake of metals by roots and low translocation into
foliage is the most common resistance trait [30]. The
mulch cover is supposed to restrict the metal uptake of
seedlings by orientation of their roots into this layer
containing less metals and to protect plant roots from
drought and to provide a source of nutrients [17,31].
However, our results are not in agreement with these
Figure 5. Mean Cu and Ni concentrations in rootsf pine
and birch by treatments, n = 3. The bar indics the
standard error of the mean.
Figure 6. Vertical distribution of mean exchangeable Cu
and Ni in the soil profile by treatments, n = 3. The bar
indicates the standard error of the mean. Please, note the
different scale of the vertical axis for Cu and Ni.
Copyright © 2013 SciRes. OJAP
earlier findings. We found no enhancement of biomass
production by mulching, and the mulch layer did not
decrease the availability of Cu and Ni to the seedlings. In
contrast, the Cu concentrations in birch wood increased
by the mulch treatment. As the root Cu concentration did
not increase, the results suggest increased root-to-shoot
mobility of Cu due to mulching. It appears that some of
the Cu com- pounds formed through complex formation
by organic molecules supplied by mulching would be
more readily translocated from birch root to shoot than
the Cu forms at the control plots.
4.2. Soil Extraction as a Predictor of Cu:Ni
hch is
concentrations from 1 to 262
g a mulch layer on metal availability
species dependent. The mulching
art of the research project
osystem from Long-Term
[1] E. Mälkönen, .-S. Helmisaari, M.
Kukkola, M. K. Salemaa, “Com-
Uptake Ratio
Clearly more Cu than Ni was taken up by pine, wi
in agreement with the higher Cu concentrations in rela-
tion to the Ni concentrations measured from the soil
samples. However, the soil Cu concentrations were al-
most 10 times higher than the soil Ni concentrations,
while the wood Cu concentrations of pine were only 3
times higher than those of Ni. In birch, the Cu and Ni
concentrations in the wood of the control seedlings were
equal and in the mulch treated seedlings the Cu concen-
trations were only twice as high as those of Ni. Hence,
the BaCl2 + EDTA extraction schema used by us as soil
extraction method appeared to give an underestimation of
both the birch and pine available amount of Ni in relation
to Cu. The BaCl2 method is reported to give an indication
of immediately exchangeable metals [32,33], while the
use of EDTA has been reported to give a good estimation
of potentially plant available metal fractions [34].
4.3. Surface Deposition Affected Cu and Ni
The Cu and Ni concentrations in the compartments s
jected directly to aerial deposition (bark, young shoots,
and foliage) were clearly higher than those of wood and
roots. A high proportion of these metal concentrations is
caused by aerial deposition of dust that accumulates on
the plant surfaces and do not penetrate into the living
tissues [18,35,36]. Thus, high amounts of heavy metals
on plant surfaces do not necessarily pose any acute toxic
hazard to plant metabolism.
Tree bark is known to sorb and accumulate airborne
contaminants and therefore, it has been largely used for
monitoring of atmospheric pollution [37-39]. In our study
the whole bark layer, including the living inner bark, was
taken by peeling it completely from the tree shoots. The
inner bark metal concentrations reflect the phloem sap
flow. The Cu and Ni concentrations in the bark obtained
in our study are roughly hundreds of times higher than
the nationwide mean values (3.6 and 1.1 mg·kg1, re-
spectively) reported by Lippo et al. [35]. Also Saarela et
al. [39] found lower metal concentrations (Cu 89 mg·kg1
and Ni 18 mg·kg1) than our values in Scots pine bark
sampled during forest felling 6 kilometers northeast from
the Harjavalta smelters.
Scots pine needle Cu concentrations ranging from 1.7
to 270 mg·kg1 and Ni
g· k g 1 have been found in a 350 km-long transect ex-
tending from the Monchegorsk smelter complex, NW
Russia, through Finnish Lapland to the Finnish-Swedish
border [40-43]. We found even higher concentrations, Cu
ranging from 100 - 600 mg·kg1 and Ni from 50 - 140
mg· k g 1 in our study than the values reported from the
Kola gradient.
5. Conclusion
The effect of addin
to tree seedlings was
had no clear effect on the Cu and Ni availability to pine,
while Cu uptake by birch was enhanced on the mulch
treated plots. In addition, although generally more Cu
than Ni was taken up by the tree seedlings, the Ni uptake
rate was higher than what could be predicted on the basis
of the ratio of soil exchangeable Cu and Ni concentra-
6. Ack
The present study formed a p
Recovery of Boreal Forest Ec
Heavy-Metal Pollution coordinated by Heljä-Sisko Helmi-
saari at Metla and was partly financed by the Academy
of Finland. The authors are grateful to several researchers
and staff at Metla for laboratory analysis and assistance
in field sampling and production of graphics. We are
especially grateful to Oili Kiikkilä, Christian Uhlig, Anne
Siika and Sari Elomaa. The work of Eva Komanická has
been supported by APVV-0231-07 and UK 373/2012.
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