Tree Physiology 17, 697--703
© 1997 Heron Publishing----Victoria, Canada
Distribution of elements along the length of Scots pine needles in a
heavily polluted and a control environment
M. J. GIERTYCH,1 L. O. DE TEMMERMAN2 and L. RACHWAL1
1
Polish Academy of Sciences, Institute of Dendrology, Parkowa 5, PL-62-035 Kórnik, Poland
2
Institute for Chemical Research, Leuvensesteenweg 17, 3080 Tervuren, Belgium
Received July 11, 1996
Summary Pollution often causes visible symptoms of foliar
injury. The injury is sometimes associated with an increase in
the accessibility of toxic elements to plants as a result of
acidification of the soil. We investigated the distribution of
elements (N, P, K, Ca, Mg, Mn, S, Fe, B, Cu, Zn, Al, F, Pb, Cd,
Cr, Ni and Co) in healthy current-year needles of Scots pine
(Pinus sylvestris L.) growing at an unpolluted control site and
at a site polluted mainly by SO2, HF and Al3+ from a fertilizer
factory established in 1917. Needles from both sites were
sampled before the appearance of visible injury and cut into
five sections of equal length (tip, base and three middle parts).
The mean concentrations of major nutrients were 20--30%
lower in needles at the polluted site than in needles at the
control site, whereas the concentrations of aluminum and fluorine were higher in needles at the polluted site. An increase in
concentration from needle base to tip was detected for N, Fe,
B, and Al at both sites and for Mn only at the polluted site.
Fluoride accumulated in the tips of needles only at the polluted
site, which could explain the necroses of needle tips at this site.
The distribution of elements along the length of the needles
was influenced by pollution, element mobility and the distal
accumulation of toxic elements.
Keywords: chemical elements, needle part, nutrients, Pinus
sylvestris, pollution.
Introduction
There have been many analyses of the chemical composition
of Scots pine needles. As a result, we know the ranges of
optimal concentration for particular elements, the thresholds
of toxicity for some elements (Fober 1993) and the symptoms
of nutrient deficiency as well as the influence of fertilization
(Baule and Fricker 1973). The accumulation of elements in
plant leaves is a dynamic process that is coupled with other
metabolic processes occurring in the plant. Element concentrations are also influenced by many factors including foliar age,
time of year, and environmental conditions (e.g., edaphic quality and pollution level) at the site (van den Driessche 1974,
Ostrowska and Szczubialka 1988, Heliövaara and Väisänen
1989).
In Pinus species, the effects of growing season, origin of
seed source, age of needles and position on tree crown on
changes in element concentrations are well documented (Will
1957, Giulimondi and Duranti 1975, Fober 1976, Helmisaari
1990, Heisendorf et al. 1993). Because many papers have
shown that pollution alters nutrition and the concentration of
elements in needles (Skeffington and Roberts 1985, Reich et
al. 1988, Heliövaara and Väisänen 1989, Holopainen and Nygren 1989, Raitio 1990, Baker et al. 1994, Shaw and McLeod
1995), the chemical composition of needles is frequently used
to monitor environmental pollution (Dmuchowski and Bytnerowicz 1995). In all of the studies of pollution cited above,
the mean concentrations of elements in whole needles were
usually determined; however, the appearance of the visible
injuries suggests that the high concentration of elements associated with injury or symptoms of deficiency occur only in
particular parts of needles. So far, only the work of Jamrich
(1972) describes the concentrations of several elements in
different parts of needles injured by fluorine emissions.
Therefore, the aim of this study was to determine whether
there is an accumulation of toxic elements in the part of healthy
needles where necroses often appear. We also assessed the
influence of pollution on the distribution of chemical elements
along the length of the needle. We analyzed needles without
visible injuries, to determine how the elements were distributed before the appearance of necroses. The study was conducted with healthy current-year needles of Scots pine (Pinus
sylvestris L.) growing at an unpolluted control site and at a
polluted site at which typical needle injuries caused by fluoride
and sulfur dioxide have been documented (Piskornik and
Godzik 1970, Horntvedt and Robak 1975, Malhotra and Blauel
1980, Oleksyn et al. 1988, Karolewski 1990, Giertych and
Werner 1996).
Materials and methods
Plant material
Current-year needles were collected after the end of the growing season in September 1994 from 12-year-old Scots pine
trees growing at two sites in western Poland. One site is located
at Luboñ near Poznañ (52°15′20″ N, 16°50′31″ E), about 2 km
698
GIERTYCH, DE TEMMERMAN AND RACHWAL
from a phosphate fertilizer factory that was established in
1917, and the other site is in the Forest Range Zwierzyniec
near Kórnik (52°14′36″ N, 17°05′00″ E), about 15 km from the
fertilizer factory and considered to be free of acute pollution
(control). Both sites have been intensively studied during the
past 12 years (Oleksyn and Bialobok 1986, Oleksyn 1988,
Reich et al. 1994, Karolewski and Giertych 1995). The polluted site has received long-term pollution in the form of
atmospheric deposition of SO2 and HF and it is also characterized by an elevated concentration of Al3+ ions in the soil
(Reich et al. 1994, Karolewski and Giertych 1995).
proportional to the length, defined as a base, tip and three
middle parts. Before cutting the needles, the fascicle sheath
was removed. The cutting occurred over several days and
during this time the needles were stored at 4 °C. The sections
from each tree were pooled separately. Needle sections were
weighed, oven dried at 65 °C, weighed again to determine the
content of water, ground and stored in plastic boxes. Each
sample (one needle section per tree) weighed more than 6 g dry
weight (gdw). The five sections were analyzed separately for all
elements except sulfur, for which three sections (tip, base and
one middle) were analyzed.
Preparation procedure
Chemical analyses
Healthy-looking, current-year needles were taken from several branches in different parts of the crown. To minimize
possible confounding effect of genetic differences, at each site,
samples were taken from three trees (replicates) from one
Polish provenance (No. 7 Spala). The needles were transported
to the laboratory in plastic bags. The needles were not washed.
Each needle was cut with a razor-blade into five equal sections
For the analysis of P, K, Ca, Mg, Mn, Fe, B, Cu, Zn, Al, Pb,
Cd, Cr, Ni and Co, the modified CII method was followed (CII
1969). Detection limits for heavy metals were 0.35 µg gdw−1 for
Cd, Cu, Cr and Co, 0.25 µg gdw−1 for Zn, and 1.25 µg gdw−1 for
Pb and Ni. Recoveries of 90--100% were obtained for several
reference plant materials: BCR 060, 061, 062 and NIST 1570,
1571, 1572, 1573, 1575. Dried and ground needles were calci-
Table 1. Summary of ANOVA for needle element concentrations, by site and needle section (df = degrees of freedom; MS = mean squares; and
P-values = probability values).
Source of variation
Site
Tree (Site)
Sections
Site × Section
Error
Element
N
P
MS
P
MS
P
MS
P
MS
P
1
4
4
4
16
89399000
4137000
14852000
1035500
721100
0.0097
397060
129300
24010
5574
2254
0.1546
13770000
2380000
5680800
951300
292800
0.0739
855260
78948
9785
9781
3216
0.0302
0.0000
0.2676
1
0.0000
0.0394
S (inorganic)
0.0482
0.0483
S (organic)
df1
MS
P
MS
P
MS
P
MS
P
1 (1)
4 (4)
4 (2)
4 (2)
16 (7)
9785800
3025000
1266300
105500
48014
0.1465
225.9
7.3
108.4
9.1
9.9
0.0052
207100
117100
97128
35067
85472
0.2543
131500
1105000
512200
902600
1445000
0.7474
0.0000
0.1155
0.0002
0.4773
Cu
0.3710
0.6762
Ni
0.7135
0.5629
Fe
df
MS
P
MS
P
MS
P
MS
P
1
4
4
4
16
324.5
26.2
59.3
5.5
10.2
0.0244
0.94
0.94
0.77
0.60
0.06
0.3738
0.31
0.82
10.46
0.29
0.51
0.5749
0.186
23.565
27.265
5.642
5.384
0.9335
0.0044
0.7102
Mn
Site
Tree (Site)
Sections
Site × Section
Error
0.0002
0.0863
B
Zn
Site
Tree (Site)
Sections
Site × Section
Error
Mg
df
Ca
Site
Tree (Site)
Sections
Site × Section
Error
K
0.0000
0.0002
Al
df
MS
P
MS
1
4
4
4
16
1651.1
657.2
2495.1
2633.0
546.7
0.1881
248510
11919
425770
124870
1177
0.0119
0.0096
0.0000
0.6852
F
P
0.0103
0.0000
0.0002
0.0079
0.4137
Ca/Al (molar)
MS
P
MS
P
1365.5
109.0
1252.8
1242.2
131.5
0.0240
1181.5
122.0
243.5
60.7
12.4
0.0358
The df for inorganic and organic S are in parentheses.
TREE PHYSIOLOGY VOLUME 17, 1997
0.0004
0.0004
0.0000
0.0091
DISTRIBUTION OF ELEMENTS ALONG SCOTS PINE NEEDLES
nated for 2 h at 450 °C. Silicates were destroyed by adding a
mixture of HF and HNO3 to the ash and evaporating (three
successive times). The residue was dissolved in HNO3 and the
concentration was measured by inductively coupled plasma
emission spectrometry (ICP).
Nitrogen was analyzed by the Kjeldahl procedure. Sulfur
was determined by ion chromatography (Dionex 2000i, Sunnyvale, CA) after differentiation of organic and inorganic sulfur by a slight modification of the procedure described by Jäger
and Steubing (1970). Total sulfur was calculated by adding
organic and inorganic sulfur.
For the determination of fluoride, dried and ground plant
material was extracted with 0.1 N HNO3 followed by the
addition of sodium citrate buffer solution. The fluoride concentration was determined with an ion selective electrode
(Roost and Sigg 1978). The detection limit for fluorides is 1 µg
gdw−1. To eliminate interactions of other elements present in the
samples, the results were calibrated against samples containing standard additions of known fluoride concentration (Jagner
699
and Pavlova 1972). All chemical analyses were conducted at
the laboratory of the Institute for Chemical Research in
Tervuren, Belgium.
Statistical analysis
Analysis of variance (ANOVA) was used to assess the influences of site, section and their interaction on chemical element
distribution (Statistix 4.0 Analytical Software, St. Paul, MN).
Sections were nested within a tree. Site and section effects
were considered to be fixed and the tree effect was considered
to be random.
Results
The distribution of most elements along the length of the
needle was similar at both sites. Statistically significant increases from base to tip sections were noted for N, Fe, B and
Al (Table 1, Figures 1a and 2b--d), whereas decreases from
Figure 1. Mean (± SE) concentrations
of macroelements (N, P, K, Mg, Ca
and S) along the length (five sections,
except only three sections for S) of
current-year needles of Scots pine
trees (n = 3) growing on polluted and
control sites.
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700
GIERTYCH, DE TEMMERMAN AND RACHWAL
base to tip were noted for P, K, Zn, and Ni and for the Ca/Al
molar ratio (Table 1, Figures 1b, 1c, 2f, 3a and 3c). There was
a significant interaction between site and needle section for K,
Mg, Mn and Cu (Table 1). The concentration of Mn was similar
along the length of needles at the control site, but in needles at
the polluted site there was an increase in Mn concentration
from base to tip (Figure 2a). Magnesium concentration decreased from base to tip in control needles, whereas it was
similar along the length of needles at the polluted site (Figure 1d). A significant interaction was also found for F which
accumulated in needle tips only at the polluted site (Table 1,
Figure 2e). There were no significant effects of site or needle
section on organic, inorganic and total S (Table 1) concentrations. The amounts of Pb, Cd, Cr and Co were below the
detection limits.
Mean needle concentrations of N, Mg, B and Zn were
significantly higher (20--30%) at the control site than at the
polluted site (Tables 1 and 2), whereas mean needle concentrations of Fe, Mn, inorganic S, organic S and total S were similar
at both sites. Mean needle concentrations of Al and F were 2.3and 23-fold higher, respectively, at the polluted site than at the
control site. The Ca/Al ratio was significantly lower at the
polluted site than at the control site (Tables 1 and 2).
Needle water contents were significantly higher at the control site than at the polluted site (53.5 ± 0.6% versus 46.8 ±
0.7%).
Discussion
Significant differences in element concentrations between
needle sections were found for several elements. An explanation of these differences is difficult because of a lack of information on potential differences in physiological processes and
nutrient requirements in particular parts of the needle. We
know that most needle cells are of similar age because most
cells are already present in the buds and spring leaf growth
occurs by elongation. However, there is little information on
the variation in longitudinal morphology of the needle, and so
Figure 2. Mean (± SE) concentrations of microelements (Mn, Fe and
B), toxic elements Al, F and Ca/Al
molar ratio along the length (five
sections) of current-year needles of
Scots pine trees (n = 3) growing on
polluted and control sites.
TREE PHYSIOLOGY VOLUME 17, 1997
DISTRIBUTION OF ELEMENTS ALONG SCOTS PINE NEEDLES
701
Table 2. Mean (SE) concentrations (µg gdw−1) of elements and molar
ratio of Ca/Al in whole needles of Scots pine from a control and
polluted site.
Figure 3. Mean (± SE) concentrations of heavy metals (Zn, Cu and Ni)
along the length (five sections) of current-year needles of Scots pine
trees (n = 3) growing on polluted and control sites.
it is impossible to relate observed differences in the concentration of elements along the needle length with reference to its
morphology and development.
For the elements classified as mobile, N, K, B, Zn, Ni and
Mn (Helmisaari 1990, Kabata-Pendias and Pendias 1993),
differences along the needle length could be the result of
accumulation or retranslocation which occurs late in the growing season (Helmisaari 1992). The elements classified as immobile Ca, Fe and organic S did not exhibit significant
differences in concentration between base and tip parts of the
needle except for a lower concentration of Fe in the base
section. This could be explained by a lower concentration of
chlorophyll in this part of the needle, which is normally covered by the needle sheath.
Element
Control
Polluted
N
P
K
Mg
Ca
S total
S (inorganic)
S (organic)
B
Zn
Cu
Ni
Fe
Mn
Al
F
Ca/Al
15388 (536)
1399 (29)
6101 (355)
859 (42)
2955 (259)
6371 (776)
1399 (11)
4972 (636)
17.9 (1.4)
24.5 (1.2)
1.70 (0.13)
1.19 (0.30)
21.7 (0.8)
125.3 (5.2)
134 (12)
0.60 (0.21)
17.3 (2.8)
11936 (346)
1169 (46)
4746 (235)
521 (13)
1813 (120)
5813 (356)
1120 (44)
4693 (340)
12.4 (1.0)
18.0 (1.0)
1.34 (0.17)
1.39 (0.39)
21.5 (0.9)
110.5 (10.7)
316 (34)
14.09 (7.46)
4.8 (0.8)
Fluorides accumulated in the tip of the healthy needles,
which is where necroses often occur (Jamrich 1972, Horntvedt
and Robak 1975, Malhotra and Blauel 1980). We postulate that
the accumulation of highly toxic fluoride in the needle tips and
the subsequent development of necroses in this area reduces
the influence of this element on the healthy part of needles.
Jamrich (1972) found the highest concentration of fluorides in
the discolored bands separating the green part of needles from
necroses, suggesting that F accumulates in the part of the
needle that aborts first.
The concentration of Al exhibited a linear increase from
base to tip. This pattern could be associated with the translocation of Al in the transpiration stream. Cronan and Grigal (1995)
identified four measurements that indicate threshold conditions for Al-induced stress in forest trees. One of these measurements is the foliar tissue Ca/Al molar ratio of ≤ 12.5
indicating 50% risk of Al-induced damage (cf. Rengel 1992).
The Ca/Al ratio is also positively correlated with the rate of
photosynthesis (Reich et al. 1994). In our study, the Ca/Al
molar ratio decreased from the base to the tip of needles at both
sites. For control needles, the values were 31.7 (base); 17.4;
11.6; 10.8; 12.0 (tip) and the corresponding values for polluted
needles were 10.5 (base); 4.4; 3.0; 3.0; 2.8 (tip). Thus, the
Ca/Al molar ratio was below the threshold value throughout
the length of needles at the polluted site and in the distal half
of needles at the control site.
The different distributions of Mn at the two sites----a similar
concentration in all parts of control needles and an increase in
concentration from base to tip in polluted needles----could be
associated with the distribution of Al in the needles. According
to Kabata-Pendias and Pendias (1993), an overabundance of Al
can increase absorption of other cations, particularly Mn.
However, Oleksyn et al. (1995) found that the presence of
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702
GIERTYCH, DE TEMMERMAN AND RACHWAL
aluminum in solution reduced root and needle concentrations
of Mn of hydroponically grown Scots pine seedlings.
At both sites, mean concentrations of the macroelements N,
P, K, and Ca were in the usual range for this species in Poland
(Fober 1976, 1993, Czarnowska and Stasik 1987, Kucaba
1987). In contrast, the concentration of Mg at the polluted site
was very low and may be insufficient for normal growth
(Ingestad 1979). According to Fober (1993), changes caused
by deficiency of N, Ca, Fe or B are visible in whole needles,
whereas changes caused by deficiency of K, P, Mg or Mn are
only visible at the needle tip. We observed that concentrations
of Ca and Fe were evenly distributed along the length of the
needles, whereas concentrations of K and P were lower in
needle tips than in other parts of the needle. The concentrations
of some microelements (Fe, Zn, B, S, Mn) were very low at
both sites and well below toxic concentrations (Kabata-Pendias and Pendias 1993). Only F at the polluted site occurred at
concentrations considered toxic.
Needle concentrations of N, K, Mg, B, and Zn were significantly higher at the control site that at the polluted site. This
difference may be related to the lower water content of polluted needles and associated differences in senescence processes between sites. During senescence the concentration of
water in needles decreases (Zelawski 1967) as do the needle
concentrations of N and K (Helmisaari 1992). An alternative
explanation for the significantly higher concentrations of major elements at the control site than at the polluted site may be
associated with the more acidic soil at the polluted site compared to the control site, pH 4.2 versus 5.8 (Reich et al. 1994).
On acidic soils, accessibility of Al for plants is increased and
aluminum limits the uptake of macroelements and some microelements (Kabata-Pendias and Pendias 1993).
We conclude that many elements are unevenly distributed
along the length of Scots pine needles. The distribution patterns can be influenced by pollution, by differences in the
mobility of elements and by the distal accumulation of toxic
elements. The distribution of some elements was associated
with subsequent injury or deficiency symptoms. Because
chemical analyses of whole needles may underestimate element concentrations in particular needle parts, it is important
to identify which part of the needle is used for analysis,
particularly when conducting bioindication analyses. Differential distribution of chemical elements along the length of the
needle can also influence physiological and biochemical processes and it is necessary to examine this subject.
Acknowledgments
The authors thank A. Niemir and R. Zytkowiak for help in fieldwork
and sample preparation, and M. Hoeing, P. Coosemans, R. Van Cauter
and H. Baeten for help in conducting laboratory analyses. We are also
grateful to Mark G. Tjoelker, Jacek Oleksyn and Piotr Karolewski for
helpful comments on earlier versions of this manuscript.
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