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Seasonal variations of nickel concentrations in annual xylem rings of beech trees (Fagus sylvatica L.)
the Science of the Total Environment The Science of the Total Environment 145 (1994) 111-118
ELSEVIER
Seasonal variations of nickel concentrations in annual xylem rings of beech trees (Fagus sylvatica L.) Jfirgen Hagemeyer*, Hartmut Schfifer, Siegmar-W. Breckle Bielefeld University, Faculty of Biology, Department of Ecology, D-133615 Bielefeld, Germany (Received 21 November 1992: accepted 28 January 1993)
Abstract Seasonal variations of Ni concentrations in stem wood of mature beech trees (Fagus sylvatica L.) were detected. Wood samples were collected at monthly intervals between April and December from trees of two sites in Germany. Radial distribution patterns of Ni were similar in all trees. Highest contents were found in the sapwood. Lower concentrations occurred in the outer heartwood. Towards the stem center, Ni levels increased. The general profile of such radial patterns did not change substantially during the period investigated. However, the concentration levels of Ni varied significantly with the season. Highest Ni concentrations were found in April. Variations between June and December were less significant. The presented results suggest, that radial distribution patterns of Ni in xylem rings of beech trees do not contain a reliable record of the Ni availability during the life span of the trees. The reasons are: (a) The distribution patterns showing high levels near the sapwood-heartwood transition indicate the possibility of a radial transport of Ni and a subsequent accumulation in the inner sapwood. (b) Seasonal variations of Ni concentrations in wood render the analytical data useless for the reconstruction of pollution levels in the past.
Key words." Fagus; Nickel; Tree rings; Sapwood; Heartwood
1. Introduction The element nickel has been considered as a potential pollutant of the environment for some time (Schmidt and Andren, 1980). Sources o f Ni pollution are: metal processing works, the combustion of Ni containing fossil fuels, and the deposition o f sewage sludge (Kabata-Pendias and Pendias, 1984). The essentiality of Ni for plant * Corresponding author.
growth is still under discussion (Welch, 1981; Eskew et al., 1984). Some beneficial effects o f low concentrations were shown in certain species (Mishra and Kar, 1974). Nickel is widely distributed in the environment with average soil concentrations ranging between 17 and 1700 /~mol/kg (Kabata-Pendias and Pendias, 1984). On serpentine rocks the Ni concentrations in soils and plants can be considerably higher (Menezes de Sequeira and Pinto da Silva, 1992). Hyperaccumulating plants, like some Alyssum species can have Ni con-
0048-9697/94/$07.00 © 1994 Elsevier Science B.V. All rights reserved. SSDI 0048-9697(93)03660-T
112
centrations in their leaves of > 17 000 ~mol/kg (Brooks, 1980; Morrison et al., 1980; Adriano, 1986). Nickel is readily absorbed by plant roots and is highly mobile in plants (Cataldo et al., 1978a,b; Burton et al., 1983; K6rner et al., 1986). In the xylem, Ni is transported as an organic complex (Cataldo et al., 1988). There is only scant information on Ni concentrations in stem wood of trees. Meisch et al. (1986) found Ni concentrations of 1.7-66 #mol/kg dry wt. in stem wood of mature beech trees in Germany. In wood of southern red oak trees growing in the USA, Gilfrich et al. (1991) determined Ni levels of 78-255/~mol/kg. In some investigations Ni concentrations were determined in single annual growth rings of different years. The measured concentrations were plotted along a time axis showing the year of wood growth. The resulting radial distribution patterns of Ni and other trace elements in wood were tentatively used as a source of information about pollution levels of the tree's environment in the past (Burton, 1985; Hagemeyer, 1993). However, it is not clear whether the described method of biomonitoring, named dendroanalysis, can yield correct results (Barnes et al., 1976; Kazmierczakowa et al., 1984; Hagemeyer and Breckle, 1986; Hagemeyer et al., 1992). Several dendroanalytical studies were conducted with the element Ni. Meisch et al. (1986) observed no chronological tendency in the Ni distribution patterns of beech in Germany. In pine trees (Pinus sylvestris) in southern Germany, increasing Ni concentrations were found in wood of recent years (Tendel and Wolf, 1988). These rises were attributed to both increased emissions of the element and enhanced Ni uptake as a result of soil acidification. A study of element distribution in annual rings of Korean pine (Pinus koraiensis) and Mongolian oak (Quercus mongolica) in north-east China showed similar radial Ni patterns in both species (Chun and Hui-yi, 1992). Average Ni concentrations in wood of the last 200 years were circa 19 #mol/kg dry wt. in both species. The rather even patterns were in accordance with the known stability of the environment in that region during the investigated period. In the USA, the distribution of Ni in annual
J. Hagerneyer et al. / Sci. Total Environ. 145 (1994) 111-118
xylem rings of various tree species growing on sites with contaminated groundwater was studied by Yanosky and Vroblesky (1992). The measured Ni concentrations in the wood were correlated with the Ni levels of the groundwater at the respective sites. As the authors did not find indications for an across-ring mobility of Ni in the xylem, they concluded, that the dendroanalytical method is suitable for tracing the history of Ni pollution in an area. There are several basic requirements to be met before an interpretation of radial element distribution patterns in tree stems in terms of pollution chronologies is possible (Hagemeyer, 1993). First of all, it must be established, that a once deposited distribution pattern of an element in tree rings does not change its shape in later periods of time. Furthermore, the patterns of neighbouring trees growing in the same environment should display, at least, similar tendencies (Hagemeyer, 1993). In order to find out whether these requirements are fulfilled in the case of Ni, the distribution patterns in stems of mature beech trees from two sites in Germany were investigated. Of particular interest were (a) the concentration levels of Ni in beech wood from different sites, (b) the radial distribution in relation to the sapwood-heartwood boundary, and (c) possible seasonal variations of Ni distribution patterns.
2. Experimental 2.1. Investigated sites and trees Samples of stem wood were collected from 10 mature beech trees (Fagus sylvatica) growing at two sites in northern Germany. One site was a 95year-old beech forest near Schwaney (Eggegebirge, 380 m a.s.1.). The region is moderately polluted by emissions carried along with westerly winds from the Rhein/Ruhr industrial area (Gehrmann, 1987). The other site was a ll5-year-old beech forest located near Glindfeld (Rothaargebirge, 700 m a.s.l.). The pollution level is considerably lower compared with Schwaney.
2.2. Sampling procedure Wood samples were obtained from the stems with an increment borer (30-cm long, 0.5-cm core
J. Hagemeyer et al. / Sci. Total Environ. 145 (1994) 111-118
diameter, Teflon coated, Model Suunto) at about 1.5 m above ground. In order to investigate seasonal variations in Ni distribution patterns, the same trees were sampled eight times at monthly intervals between April and December (Breckle and Hagemeyer, 1992). Data are presented for four sampling dates: 4th April, 9th June, 5th September and 4th December 1987. In order to avoid disturbances of Ni distributions caused by the previous drillings, later samples were taken from slightly different directions and heights of the stem. Cores were extracted - 2 0 cm above or below the older holes and in a horizontal distance of 10 cm. The holes were sealed with tightly fitting wood plugs and wax to minimize damage to the living tree. The borer was cleaned and disinfected with isopropanol before each use. After the extraction, wood cores were instantly frozen in liquid nitrogen and stored in a freezer to avoid lateral movement of ions. In the laboratory, the extent of sapwood was determined by the starch content of the xylem. Small chips of wood were cut off from different parts of the cores with a sharp blade for the staining with iodine in potassium iodide solution. Sapwood was defined as that part of the wood, that contained detectable amounts of starch. The transition between sapwood and heartwood was determined separately for each of eight individual wood cores of each tree. The mean values were assumed to represent the approximate location of the boundary. In the illustrations the sapwood-heartwood transition zone is indicated by the limits of ±1 standard deviation of the means of eight determinations.
2.3. Chemical analyses q[" wood The wood samples were freeze-dried and then dried in an oven at 105°C to constant weight. The wood cores were divided into smaller segments including five or ten annual growth increments. These were digested under pressure with concentrated H N O 3 in teflon vessels at 150°C. Concentrations of Ni were determined by graphite furnace atomic absorption spectrophotometry (PerkinElmer 5100 fSberlingen, Germany). The results were calculated on wood dry weight basis. In order to check the quality of the analytical procedure, NBS Standard Reference Material
113
1571 (Orchard leaves) was analyzed. The certified concentration of Ni is 1.30 ± 0.2 ppm. Using the above described procedure, 1.21 ± 0.14 ppm Ni (n = 11) were found, i.e. 93.1% of the required concentration. Average Ni concentrations of 23 blanks were 0.29 ± 0.54 ppb. The detection limit was defined as 3 x the standard deviation of the blank values (Stoeppler, 1985), i.e. 1.61 ppb Ni. When calculated on wood dry weight basis, this means for an average sample weight of 0.2 g wood there is a detection limit of 41.8 ppb or 0.71 p,mol Ni/kg wood dry wt.
2.4. Soil parameters In each of the investigated beech forests, l0 soil samples were collected from the upper layer (0-5 cm depth) and from a lower horizon (10-20 cm). Soil samples were dried at 60°C and twice passed through a screen (2 mm and 0.2 mm mesh). The material was digested with concentrated HNO3, like wood samples, in Telfon pressure vessels. The Ni concentrations (AAS) are refered to as 'total contents' of the soil. Furthermore, extractable Ni concentrations were measured in extracts of 1 M ammonium acetate at pH 7 (soil: extractant ratio 1:10, 2 h on a shaker). The results are presented as mean values for each site (Table 1). The pH values of the soil in Glindfeld were determined in 0.1 M KCI with a soil/solution ratio of 1:2.5. The pH values of Schwaney were provided by J. Gehrmann (pers. commun.). 2.5. Statistical treatment of data For the comparison of mean values an analysis of variance including the Scheff~ test was conducted. 3. Results
3.2. Nickel levels in soils and stem wood o[ beech trees The soil of the forest stand in Schwaney contained more Ni than that found at Glindfeld (Table 1). In particular the extractable concentrations of the samples from Schwaney considerably exceeded those from Glindfeld. Such differences were reflected by the Ni concentrations found in
J. Hagemeyer et al./Sci. Total Environ. 145 (1994) 111-118
114 Table l Concentrations of Ni and pH of the soils of the investigated sites in Germany
--t~-- April - o 7 C~
Site
Schwaney Glind~ld
Soil depth (cm)
Ni (#mol/kg soil dry wt.) Extract
Total
0-5 10-20 0-5 10-20
8 10 3 1
660 820 500 560
pH (KCI)
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The extractable fraction of Ni was determined from extracts of 1 M ammonium acetate. Approximate total contents were measured in samples digested with concentrated nitric acid. Data are means of 10 samples: pH values of Schwaney provided by J. Gehrmann (pers. commun.)
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Year Fig. I. Radial distribution of Ni in stem wood of beech tree No. 1 (Fagus sylvatica) in Schwaney, Germany. Samples were taken between April and December 1987 at 1.5 m above ground. The broken vertical lines delimit the transition zone between sapwood and heartwood.
the wood of beech trees of both sites (Table 2). Mean Ni concentrations in stem wood were significantly higher (P < 0.01) in Schwaney (30.58 ± 5.36 ~tmol/kg wood dry wt., n = 5) than in Glindfeld (17.45 ± 5.08/xmol/kg wood dry wt., n=5).
sapwood. Lowest Ni concentrations occurred in the region of the sapwood-heartwood transition (Figs. 2, 4 and 6) or in the outer part of the heartwood (Figs. 1, 3 and 5). A distinct increase of the concentrations towards the stem center, the pith, was observed in all investigated beech trees. This pattern was found in trees of both sites. In Schwaney, however, the differences between highest and lowest Ni concentrations within a tree were
3.2. Radial distribution of nickel The radial Ni distributions in stem wood of mature beech trees showed a characteristic pattern (Figs. 1-6). Highest concentration levels were generally encountered in the central part of the
Table 2 Mean concentrations of Ni in stem wood of beech trees of two sites in Germany Site
Tree
Ni (#mol/kg wood dry wt.) April
June
September 6.6b 10.8a 9.6ab 17.4a 9.8b
24.4 30.3 32.5 35.6 19.1
± ± ± + +
8.lab 17.4a 6.2ab 16.3a 11.9b
2.0b 4.8ab 3.0b 4.5ab 4.5ab
7.5 19.4 15.0 17.2 11.2
+ + ± ± ±
2.1b 4.3b 2.3b 2.3b 2.4b
Schwaney
1 2 3 4 5
36.7 39.5 43.2 43.5 37.4
± ± ± ± ±
12.4a 15.0a 7.1a 15.6a 12.0a
18.9 21.3 28.6 31.0 26.9
± ± ± ± ±
5.5b 10.5a 9.3b 9.4a 12.5ab
19.7 26.3 32.6 39.7 19.6
+ ± ± + ±
Glindfeld
1 2 3 4 5
17.4 33.0 24.1 25.2 18.0
± ± :i: ± ±
2.1a 10.5a 6.4a 5.1a 3.3a
9.3 19.4 12.7 18.0 17.0
± + ± ± ±
2.3b 10.2b 6.3b 5.1b 5.4ab
10.5 24.6 13.7 22.1 13.0
+ + ± ± ±
December
Wood samples were collected in 4 different months in 1987 from each tree at 1.5 m height. Data are means ± S.D. of 8-14 wood samples located along radii extending from cambium to pith (cf. Figs. 1-6). Values in each line followed by the same letter do not differ significantly at the P = 0.01 level.
J. Hagemeyer et al. / Sci. Total Environ. 145 (1994) 111-118 --I,-- April 70
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Year Fig. 2. Radial distribution o f Ni in stem wood o f beech tree No. 2 in Schwaney, Germany. For further details see Fig. ].
Fig. 4. Radial distribution of Ni in stem wood of beech tree No. 4 in Schwaney, Germany. For further details see Fig. 1.
larger and, thus, the radial distribution patterns were more pronounced.
peaks and troughs was not observed. This was also true for the trees in Glindfeld (data not shown). Whereas the distribution patterns were stable in shape, concentration levels of Ni showed marked variations with the season. Highest Ni concentrations were often encountered in the samples collected in April (Table 2). April values were significantly higher than June values (P < 0.01 ) in two trees of Schwaney (nos. 1, 3) and in four trees of Glindfeld (nos. 1-4). The differences between the other months, i.e. June, September and December, were much smaller and rarely significant. In the
3.3. Seasonal variability of nickel distributions In order to investigate the stability of the described Ni patterns, the distributions were determined in the same trees in different months of 1 year (Figs. 1-5). The general patterns of Ni distribution in stem wood did not change considerably during the investigated period between April and December. Alterations in the radial Ni profiles were only of minor scale. A radial displacement of
--A-- April
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Year Fig. 3. Radial distribution of Ni in stem wood of beech tree No. 3 in Schwaney~ Germany. For further details see Fig. I.
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Year Fig. 5. Radial distribution o f Ni in stem wood o f beech tree No. 5 in Schwaney, Germany. For further details see Fig. 1.
J. Hagemeyer et al./Sci. Total Environ. 145 (1994) l l l - l l 8
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Year Fig. 6. Radial distribution of Ni in stem wood of 5 beech trees in Glindfeld, Germany. Data points represent means of 8 samples collected from the same tree at monthly intervals between April and December 1987. The small bars in each curve denote the center of the individual sapwood-heartwood transition. The broken vertical lines indicate the approximate range of the sapwood-heartwood transition zone for all trees which have a similar age.
tree Glindfeld 1, September values of Ni were significantly higher than December levels (P < 0.05) and in tree Glindfeld 5, June values were higher than those of December (P < 0.05). In two trees, no significant differences at all were found in the Ni levels of the four investigated months (Schwaney 2 and 4). 4. D i s c u s s i o n
Nickel concentrations in stem wood of beech trees from two sites in Germany showed distinct radial distribution patterns. Highest levels were observed in the middle part of the sapwood. The general shape of such radial distribution patterns was preserved during one vegetation period between April and December. However, the concentration levels, showed marked seasonal variations; highest Ni concentrations were generally found in samples collected before bud break, in April. During and after the vegetation period, Ni levels in stem wood were lower and more stable. The results indicate redistributions of Ni in stem wood of beech trees during the course of 1 year. Seasonal variations of various elements in xylem
sap of mature beech trees, e.g. Cd, Ca, Mg, K and Mn were reported by Glavac et al. (1990a,b). The observed concentration changes were apparently related to variations in the physiological status of the trees during the year. Highest levels of Cd, Ca and Mn were determined during the spring mobilization period in April. This agrees with our observation of highest Ni concentrations in the wood at the same time (Table 2). The presented Ni concentrations in wood, which were determined after wet ashing of the material, are total contents. They represent combinations of different fractions of the element, which occur in the xylem tissue. Part of the Ni is readily mobile in xylem sap. Another fraction is probably bound as Ni ions by electrostatic force to fixed negative charges in the xylem vessel walls. This was described for Ca, Cd and other cations as well (Ferguson and Bollard, 1976; Petit and Van de Geijn, 1978; McGrath and Robson, 1984). Binding to fixed negative charges is a reversible process. The Ni ions can be exchanged against other ions and become remobilized, whenever the ionic composition or the pH of the xylem sap have changed. This will occur in connection with physiological processes during the annual cycle of growth in deciduous plants (Ferguson et al., 1983). After their release, the ions are transferred in the xylem sap stream into other parts of the tree. A basipetal transport is possible in the phloem elements (Hill, 1980; Neumann and Charnel, 1986). Such circulation processes can explain the observed variations of Ni concentrations in the wood. The radial distributions of elements in stem wood were shown to depend in part on the cation exchange capacity of the tissue. In stem wood of Picea rubens, the density of fixed negative charges in cell walls varies on the radius of the stem (Momoshima and Bondietti, 1990). The highest charge density was observed in the stem center. The measured increase in Ca concentrations towards the stem center was attributed to the increased binding capacity of the wood. Also the Ni concentrations in beech wood showed higher values near the center of the stem (Figs. 1, 2, 4 and 5). It is not known, whether this is actually related to the cation binding capacity of the xylem. |t seems, however, likely, that the cation exchange
J. Hagemeyer et al./Sci. Total Environ. 145 (1994) 111-118
capacity of the wood tissue will affect the distribution of nickel. A pathway for radial transport of mineral elements within the stem are the rays. They consist of strands of living cells, extending radially through the xylem tissue. The movement of mineral nutrients in the rays was described by Ziegler (1968). Nutrients, like P, K and S are apparently transported towards the outer annual rings where they are used in living cells. Other elements, e.g. Ca, seem to be transported into the inner parts of the stem. Such processes can also influence the distribution of Ni in stem wood. The highest contents were found in the sapwood, close to the transition to heartwood (see Fig. 1). This distribution can be caused by a centripetal transport process in connection with heartwood formation. It was suggested, that the conversion of sapwood into heartwood is linked to a centripetal transport of physiologically useless waste substances in the rays (Stewart, 1966). The accumulation of toxic waste, including trace metals, can cause the death of ray cells and the formation of heartwood. Thus, the Ni peak in the older sapwood of beech trees may result from a centripetal transport of the toxic element towards the sapwood-heartwood transition. Here the ray cells are dying from a build-up of toxic material and the transport is interrupted. A similar mechanism was assumed to operate in oak trees (Quercus robur, Q. petraea), in which the highest concentrations of Cd were also found in the inner sapwood (Hagemeyer and Breckle, 1986). The hypothesis outlined suggests, that trees may even show an accelerated conversion of sapwood into heartwood under conditions of severe trace element pollution. An influence of the sapwood-heartwood transition on radial distribution patterns of elements in the trunks was described for a variety of tree species, including Fagus sylvatica (Hagemeyer et al., 1992), Fagus grandifolia (Brownridge, 1984), Quercusmongolica and Pinus koraiensis (Chun and Hui-yi, 1992) and Cryptomeria japonica (Okada et al., 1987). Physiological processes can obviously affect the distribution of elements in the wood of trees. This should be considered, when radial distribution patterns are used to monitor changes in environmental pollution levels in the past. A pattern, that
117
is influenced by radial element movements cannot be used to infer the extent of trace element pollution in former years. Apparently, the measured Ni concentrations in the wood are not stable during the time between deposition in the xylem and the analysis, years later. A year-to-year chronology of Ni pollution from analytical data of annual rings of beech seems, therefore, not feasible. In order to learn more about the factors governing the Ni distribution in tree stems, it will be useful to determine the sizes and relative quantities of the different fractions of Ni occurring in wood. Particularly the magnitude of the mobile fraction in relation to the total content can give an indication of the possible extent of Ni circulation in the tree. Data of the cation binding capacity of the wood will facilitate the interpretation of radial distribution patterns of Ni and other mineral elements. Furthermore, the question of the degree of radial mobility of Ni across annual growth rings should be tackled in future investigations.
5. Acknowledgments The investigation was partly funded by a grant of the Ministerium ffir Umwelt, Raumordnung und Landwirtschaft des Landes NRW, Dfisseldorf. Our thanks are extended to Katharina Lohrie for critical remarks on the manuscript.
6. References Adriano, D.C., Trace Elements in the Terrestrial Environment. Springer, New York, 1986. Barnes, D., M.A. Hamadah and J.M. Ottaway, 1976. The lead, copper and zinc content of tree rings and bark. Sci. Total Environ., 5: 63-67. Breckle, S.W. and J. Hagemeyer, 1992. Abschlul3bericht des Forschungsvorhabens "Untersuchungen des Einflusses yon Schwermetallen (insbes. Cd, Zn) auf die Kambiumaktivitfit mitteleurop/iischer Waldb/iume (Buche, Fichte)". Forschungsberichte zum Forschungsprogramm des Landes NRW "Luftverunreinigungen und Waldschfiden", 19: 1-143. Brooks, R.R., Accumulation of nickel by terrestrial plants. In J.O. Nriagu (Ed.t, Nickel in the Environment. J. Wiley and Sons, New York, 1980, pp. 407-430. Brownridge, J.D., 1984. The radial distribution of 137Cs and 4°K in tree stems. J. Plant Nutr., 7: 887-896. Burton, MA.S., Tree rings, in Monitoring and Assessment Research Centre, Historical Monitoring. A Technical Report. University of London, 1985, pp. 175-202.
118 Burton, K.W., E. Morgan and A. Roig, 1983. The influence of heavy metals upon the growth of sitka-spruce in South Wales forests. I. Upper critical and foliar concentrations. Plant Soil, 73: 327-336. Cataldo, D.A., T.R. Garland and R.E. Wildung, 1978a. Nickel in plants. I. Uptake kinetics using intact soybean seedlings. Plant Physiol., 62: 563-565. Cataldo, D.A., T.R. Garland and R.E. Wildung, 1978b. Nickel in plants. I!. Distribution and chemical form in soybean plants. Plant Physiol., 62: 566-570. Cataldo, D.A., K.M. McFadden, T.R. Garland and R.E. Wildung, 1988. Organic constituents and complexation of nickel (1I), iron (111), cadmium (IlL and plutonium (IV) in soybean xylem exudates. Plant Physiol., 86: 734-739. Chun, L. and H. Hui-yi, 1992. Tree-ring element analysis of Korean pine (Pinus koraiensis Sieb. et Zucc.) and Mongolian oak (Quercus mongolica Fisch. ex Turcz.) from Changbai Mountain, north-east China. Trees, 6: 103-108. Eskew, D.L., R.M. Welch and W.A. Norvell, 1984. Nickel in higher plants. Further evidence for an essential role. Plant Physiol., 76: 691-693. Ferguson, I.B. and E.G. Bollard, 1976. The movement of calcium in woody stems. Ann. Bot., 40: 1057-1065. Ferguson, A.R., J.A. Eiseman and J.A. Leonard, 1983. Xylem sap from Actinidia chinensis: seasonal changes in composition. Ann. Bot., 51: 823-833. Gehrmann, J., 1987. Derzeitiger Stand der Belastung von Wald6kosystemen in Nordrhein-Westfalen durch Deposition von Luftverunreinigungen. Der Forst- und Holzwirt, 6: 141-145. Gilfrich, J.V., N.L. Gilfrich, E.F. Skelton, J.P. Kirkland, S.B. Qadri and D.J. Nagel, 1991. X-ray fluorescence analysis of tree rings. X-Ray Spectrom, 20: 203-208. Glavac, V., H. Koenies and U, Ebben, 1990a. Seasonal variation of calcium, magnesium, potassium, and manganese contents in xylem sap of beech (Fagus sylvatica L.) in a 35year-old limestone beech forest stand. Trees, 4: 75-80. Glavac, V., H. Koenies and U. Ebben, 1990b. Seasonal variation and axial distribution of cadmium concentrations in trunk xylem sap of beech trees (Fagus sylvatica L.). Angewandte Botanik, 64: 357-364. Hagemeyer, J., Monitoring trace metal pollution with tree rings: a critical reassessment. In: B. Markert (Ed.), Plants as Biomonitors. Indicators for Heavy Metals in the Terrestrial Environment. VCH-Publisher, Weinheim, 1993, pp. 541-563. Hagemeyer, J. and Breckle, S.W., 1986. Cadmium in den Jahrringen yon Eichen: Untersuchungen zur Aufstellung einer Chronologie der Immissionen. Angewandte Botanik, 60: 161-174. Hagemeyer, J., A. L/ilfsmann, M. Perk and S.W. Breckle, 1992. Are there seasonal variations of trace element concentrations (Cd, Pb, Zn) in wood of Fagus trees in Germany? Vegetatio, 101: 55-63. Hill, J., 1980. The remobilization of nutrients from leaves. J. Plant Nutr., 2: 407-444. Kabata-Pendias, A. and H. Pendias, Trace Elements in Soils and Plants. CRC Press, Boca Raton, 1984.
J. Hagemeyer et al./Sci. Total Environ. 145 (1994) 111-118 Kazmierczakowa, R., K. Grodzinska and Z. Bednarz, 1984. Content of heavy metals in xylem of 100-year-old beech (Fagus sylvatica L.) in southern Poland. Bull. Polish Acad. Sci. Biol. Sci., 32: 329-338. K6rner, L.E., I.M. Mealierand P. Jensen, 1986. Free space uptake and influx of Ni 2÷ in excised barley roots. Physiol. Plant., 68: 583-588. McGrath, J.F. and A.D. Robson, 1984. The movement of zinc through excised stems of seedlings of Pinus radiata D. Don. Ann. Bot., 54: 231-242. Meisch, H.U., M. Kessler, W. Reinle and A. Wagner, 1986. Distribution of metals in annual rings of the beech (Fugus sylvatica) as an expression of environmental changes. Experientia, 42: 537-542. Menezes de Sequeira, E. and A.R. Pinto da Silva, Ecology of serpentinized areas in north-east Portugal. In: B.A. Roberts and J. Proctor (Eds.), The Ecology of Areas with Serpentinized Rocks. A World View. Kluwer Academic Publishers, 1992, pp. 169-197. Mishra, D. and M. Kar, 1974. Nickel in plant growth and metabolism. Bot. Rev., 40: 395-449. Momoshima, N. and E.A. Bondietti, 1990. Cation binding in wood: applications to understanding historical changes in divalent cation availability to red spruce. Can. J. For. Res., 20:1840-1849. Morrison, R.S., R.R. Brooks and R.D. Reeves, 1980. Nickel uptake by Alyssum species. Plant Sci. Lett., 17: 451-457. Neumann, P.M. and A. Chamel, 1986. Comparative phloem mobility of nickel in nonsenescent plants. Plant Physiol., 81: 689-691. Okada, N., Y. Katayama, T. Nobuchi, Y. Ishimaru, H. Yamashita and A. Aoki, 1987. Trace elements in the stems of trees I. Radial distribution in sugi (Cryptomeriajaponica D. Don). Mokuzai Gakkaishi, 33: 913-920. Petit, C.M. and S.C. Van de Geijn, 1978. In vivo measurement of cadmium (ll5mCd) transport and accumulation in the stems of intact tomato plants (Lycopersicon esculentum, Mill.). Planta, 138: 137-143. Schmidt, J.A. and A.N. Andren, The atmospheric chemistry of nickel. In: J.O. Nriagu (Ed.), Nickel in the Environment. J. Wiley and Sons, New York, 1980, pp. 93-135. Stewart, C.M., 1966. Excretion and heartwood formation in living trees. Science, 153: 1068-1074. Stoeppler, M., Cadmium-Bestimmung in biologischem und Umweltmaterial. in: W. Fresenius, H. Gfinzler, W. Huber, I. Lfiderwald, G. T61g and H. Wisser (Eds.), Analytiker Taschenbilch, Band 5. Springer-Verlag, New York, 1985, pp. 199-216. Tendel, J. and K. Wolf, 1988. Distribution of nutrients and trace elements in annual rings of pine trees (Pinus silvestris) as an indicator of environmental changes. Experientia, 44: 975-980. Welch, R.M., 1981. The biological significance of nickel. J. Plant Nutr., 3: 345-356. Yanosky, T.M. and D.A. Vroblesky, 1992. Relation of nickel concentrations in tree rings to groundwater contamination. Water Resour. Res, 28: 2077-2083. Ziegler, H., 1968. Biologische Aspekte der Kernholzbildung. Holz als Roh-u. Werkstoff, 26: 61-68.
ELSEVIER
Seasonal variations of nickel concentrations in annual xylem rings of beech trees (Fagus sylvatica L.) Jfirgen Hagemeyer*, Hartmut Schfifer, Siegmar-W. Breckle Bielefeld University, Faculty of Biology, Department of Ecology, D-133615 Bielefeld, Germany (Received 21 November 1992: accepted 28 January 1993)
Abstract Seasonal variations of Ni concentrations in stem wood of mature beech trees (Fagus sylvatica L.) were detected. Wood samples were collected at monthly intervals between April and December from trees of two sites in Germany. Radial distribution patterns of Ni were similar in all trees. Highest contents were found in the sapwood. Lower concentrations occurred in the outer heartwood. Towards the stem center, Ni levels increased. The general profile of such radial patterns did not change substantially during the period investigated. However, the concentration levels of Ni varied significantly with the season. Highest Ni concentrations were found in April. Variations between June and December were less significant. The presented results suggest, that radial distribution patterns of Ni in xylem rings of beech trees do not contain a reliable record of the Ni availability during the life span of the trees. The reasons are: (a) The distribution patterns showing high levels near the sapwood-heartwood transition indicate the possibility of a radial transport of Ni and a subsequent accumulation in the inner sapwood. (b) Seasonal variations of Ni concentrations in wood render the analytical data useless for the reconstruction of pollution levels in the past.
Key words." Fagus; Nickel; Tree rings; Sapwood; Heartwood
1. Introduction The element nickel has been considered as a potential pollutant of the environment for some time (Schmidt and Andren, 1980). Sources o f Ni pollution are: metal processing works, the combustion of Ni containing fossil fuels, and the deposition o f sewage sludge (Kabata-Pendias and Pendias, 1984). The essentiality of Ni for plant * Corresponding author.
growth is still under discussion (Welch, 1981; Eskew et al., 1984). Some beneficial effects o f low concentrations were shown in certain species (Mishra and Kar, 1974). Nickel is widely distributed in the environment with average soil concentrations ranging between 17 and 1700 /~mol/kg (Kabata-Pendias and Pendias, 1984). On serpentine rocks the Ni concentrations in soils and plants can be considerably higher (Menezes de Sequeira and Pinto da Silva, 1992). Hyperaccumulating plants, like some Alyssum species can have Ni con-
0048-9697/94/$07.00 © 1994 Elsevier Science B.V. All rights reserved. SSDI 0048-9697(93)03660-T
112
centrations in their leaves of > 17 000 ~mol/kg (Brooks, 1980; Morrison et al., 1980; Adriano, 1986). Nickel is readily absorbed by plant roots and is highly mobile in plants (Cataldo et al., 1978a,b; Burton et al., 1983; K6rner et al., 1986). In the xylem, Ni is transported as an organic complex (Cataldo et al., 1988). There is only scant information on Ni concentrations in stem wood of trees. Meisch et al. (1986) found Ni concentrations of 1.7-66 #mol/kg dry wt. in stem wood of mature beech trees in Germany. In wood of southern red oak trees growing in the USA, Gilfrich et al. (1991) determined Ni levels of 78-255/~mol/kg. In some investigations Ni concentrations were determined in single annual growth rings of different years. The measured concentrations were plotted along a time axis showing the year of wood growth. The resulting radial distribution patterns of Ni and other trace elements in wood were tentatively used as a source of information about pollution levels of the tree's environment in the past (Burton, 1985; Hagemeyer, 1993). However, it is not clear whether the described method of biomonitoring, named dendroanalysis, can yield correct results (Barnes et al., 1976; Kazmierczakowa et al., 1984; Hagemeyer and Breckle, 1986; Hagemeyer et al., 1992). Several dendroanalytical studies were conducted with the element Ni. Meisch et al. (1986) observed no chronological tendency in the Ni distribution patterns of beech in Germany. In pine trees (Pinus sylvestris) in southern Germany, increasing Ni concentrations were found in wood of recent years (Tendel and Wolf, 1988). These rises were attributed to both increased emissions of the element and enhanced Ni uptake as a result of soil acidification. A study of element distribution in annual rings of Korean pine (Pinus koraiensis) and Mongolian oak (Quercus mongolica) in north-east China showed similar radial Ni patterns in both species (Chun and Hui-yi, 1992). Average Ni concentrations in wood of the last 200 years were circa 19 #mol/kg dry wt. in both species. The rather even patterns were in accordance with the known stability of the environment in that region during the investigated period. In the USA, the distribution of Ni in annual
J. Hagerneyer et al. / Sci. Total Environ. 145 (1994) 111-118
xylem rings of various tree species growing on sites with contaminated groundwater was studied by Yanosky and Vroblesky (1992). The measured Ni concentrations in the wood were correlated with the Ni levels of the groundwater at the respective sites. As the authors did not find indications for an across-ring mobility of Ni in the xylem, they concluded, that the dendroanalytical method is suitable for tracing the history of Ni pollution in an area. There are several basic requirements to be met before an interpretation of radial element distribution patterns in tree stems in terms of pollution chronologies is possible (Hagemeyer, 1993). First of all, it must be established, that a once deposited distribution pattern of an element in tree rings does not change its shape in later periods of time. Furthermore, the patterns of neighbouring trees growing in the same environment should display, at least, similar tendencies (Hagemeyer, 1993). In order to find out whether these requirements are fulfilled in the case of Ni, the distribution patterns in stems of mature beech trees from two sites in Germany were investigated. Of particular interest were (a) the concentration levels of Ni in beech wood from different sites, (b) the radial distribution in relation to the sapwood-heartwood boundary, and (c) possible seasonal variations of Ni distribution patterns.
2. Experimental 2.1. Investigated sites and trees Samples of stem wood were collected from 10 mature beech trees (Fagus sylvatica) growing at two sites in northern Germany. One site was a 95year-old beech forest near Schwaney (Eggegebirge, 380 m a.s.1.). The region is moderately polluted by emissions carried along with westerly winds from the Rhein/Ruhr industrial area (Gehrmann, 1987). The other site was a ll5-year-old beech forest located near Glindfeld (Rothaargebirge, 700 m a.s.l.). The pollution level is considerably lower compared with Schwaney.
2.2. Sampling procedure Wood samples were obtained from the stems with an increment borer (30-cm long, 0.5-cm core
J. Hagemeyer et al. / Sci. Total Environ. 145 (1994) 111-118
diameter, Teflon coated, Model Suunto) at about 1.5 m above ground. In order to investigate seasonal variations in Ni distribution patterns, the same trees were sampled eight times at monthly intervals between April and December (Breckle and Hagemeyer, 1992). Data are presented for four sampling dates: 4th April, 9th June, 5th September and 4th December 1987. In order to avoid disturbances of Ni distributions caused by the previous drillings, later samples were taken from slightly different directions and heights of the stem. Cores were extracted - 2 0 cm above or below the older holes and in a horizontal distance of 10 cm. The holes were sealed with tightly fitting wood plugs and wax to minimize damage to the living tree. The borer was cleaned and disinfected with isopropanol before each use. After the extraction, wood cores were instantly frozen in liquid nitrogen and stored in a freezer to avoid lateral movement of ions. In the laboratory, the extent of sapwood was determined by the starch content of the xylem. Small chips of wood were cut off from different parts of the cores with a sharp blade for the staining with iodine in potassium iodide solution. Sapwood was defined as that part of the wood, that contained detectable amounts of starch. The transition between sapwood and heartwood was determined separately for each of eight individual wood cores of each tree. The mean values were assumed to represent the approximate location of the boundary. In the illustrations the sapwood-heartwood transition zone is indicated by the limits of ±1 standard deviation of the means of eight determinations.
2.3. Chemical analyses q[" wood The wood samples were freeze-dried and then dried in an oven at 105°C to constant weight. The wood cores were divided into smaller segments including five or ten annual growth increments. These were digested under pressure with concentrated H N O 3 in teflon vessels at 150°C. Concentrations of Ni were determined by graphite furnace atomic absorption spectrophotometry (PerkinElmer 5100 fSberlingen, Germany). The results were calculated on wood dry weight basis. In order to check the quality of the analytical procedure, NBS Standard Reference Material
113
1571 (Orchard leaves) was analyzed. The certified concentration of Ni is 1.30 ± 0.2 ppm. Using the above described procedure, 1.21 ± 0.14 ppm Ni (n = 11) were found, i.e. 93.1% of the required concentration. Average Ni concentrations of 23 blanks were 0.29 ± 0.54 ppb. The detection limit was defined as 3 x the standard deviation of the blank values (Stoeppler, 1985), i.e. 1.61 ppb Ni. When calculated on wood dry weight basis, this means for an average sample weight of 0.2 g wood there is a detection limit of 41.8 ppb or 0.71 p,mol Ni/kg wood dry wt.
2.4. Soil parameters In each of the investigated beech forests, l0 soil samples were collected from the upper layer (0-5 cm depth) and from a lower horizon (10-20 cm). Soil samples were dried at 60°C and twice passed through a screen (2 mm and 0.2 mm mesh). The material was digested with concentrated HNO3, like wood samples, in Telfon pressure vessels. The Ni concentrations (AAS) are refered to as 'total contents' of the soil. Furthermore, extractable Ni concentrations were measured in extracts of 1 M ammonium acetate at pH 7 (soil: extractant ratio 1:10, 2 h on a shaker). The results are presented as mean values for each site (Table 1). The pH values of the soil in Glindfeld were determined in 0.1 M KCI with a soil/solution ratio of 1:2.5. The pH values of Schwaney were provided by J. Gehrmann (pers. commun.). 2.5. Statistical treatment of data For the comparison of mean values an analysis of variance including the Scheff~ test was conducted. 3. Results
3.2. Nickel levels in soils and stem wood o[ beech trees The soil of the forest stand in Schwaney contained more Ni than that found at Glindfeld (Table 1). In particular the extractable concentrations of the samples from Schwaney considerably exceeded those from Glindfeld. Such differences were reflected by the Ni concentrations found in
J. Hagemeyer et al./Sci. Total Environ. 145 (1994) 111-118
114 Table l Concentrations of Ni and pH of the soils of the investigated sites in Germany
--t~-- April - o 7 C~
Site
Schwaney Glind~ld
Soil depth (cm)
Ni (#mol/kg soil dry wt.) Extract
Total
0-5 10-20 0-5 10-20
8 10 3 1
660 820 500 560
pH (KCI)
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Year Fig. I. Radial distribution of Ni in stem wood of beech tree No. 1 (Fagus sylvatica) in Schwaney, Germany. Samples were taken between April and December 1987 at 1.5 m above ground. The broken vertical lines delimit the transition zone between sapwood and heartwood.
the wood of beech trees of both sites (Table 2). Mean Ni concentrations in stem wood were significantly higher (P < 0.01) in Schwaney (30.58 ± 5.36 ~tmol/kg wood dry wt., n = 5) than in Glindfeld (17.45 ± 5.08/xmol/kg wood dry wt., n=5).
sapwood. Lowest Ni concentrations occurred in the region of the sapwood-heartwood transition (Figs. 2, 4 and 6) or in the outer part of the heartwood (Figs. 1, 3 and 5). A distinct increase of the concentrations towards the stem center, the pith, was observed in all investigated beech trees. This pattern was found in trees of both sites. In Schwaney, however, the differences between highest and lowest Ni concentrations within a tree were
3.2. Radial distribution of nickel The radial Ni distributions in stem wood of mature beech trees showed a characteristic pattern (Figs. 1-6). Highest concentration levels were generally encountered in the central part of the
Table 2 Mean concentrations of Ni in stem wood of beech trees of two sites in Germany Site
Tree
Ni (#mol/kg wood dry wt.) April
June
September 6.6b 10.8a 9.6ab 17.4a 9.8b
24.4 30.3 32.5 35.6 19.1
± ± ± + +
8.lab 17.4a 6.2ab 16.3a 11.9b
2.0b 4.8ab 3.0b 4.5ab 4.5ab
7.5 19.4 15.0 17.2 11.2
+ + ± ± ±
2.1b 4.3b 2.3b 2.3b 2.4b
Schwaney
1 2 3 4 5
36.7 39.5 43.2 43.5 37.4
± ± ± ± ±
12.4a 15.0a 7.1a 15.6a 12.0a
18.9 21.3 28.6 31.0 26.9
± ± ± ± ±
5.5b 10.5a 9.3b 9.4a 12.5ab
19.7 26.3 32.6 39.7 19.6
+ ± ± + ±
Glindfeld
1 2 3 4 5
17.4 33.0 24.1 25.2 18.0
± ± :i: ± ±
2.1a 10.5a 6.4a 5.1a 3.3a
9.3 19.4 12.7 18.0 17.0
± + ± ± ±
2.3b 10.2b 6.3b 5.1b 5.4ab
10.5 24.6 13.7 22.1 13.0
+ + ± ± ±
December
Wood samples were collected in 4 different months in 1987 from each tree at 1.5 m height. Data are means ± S.D. of 8-14 wood samples located along radii extending from cambium to pith (cf. Figs. 1-6). Values in each line followed by the same letter do not differ significantly at the P = 0.01 level.
J. Hagemeyer et al. / Sci. Total Environ. 145 (1994) 111-118 --I,-- April 70
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Year Fig. 2. Radial distribution o f Ni in stem wood o f beech tree No. 2 in Schwaney, Germany. For further details see Fig. ].
Fig. 4. Radial distribution of Ni in stem wood of beech tree No. 4 in Schwaney, Germany. For further details see Fig. 1.
larger and, thus, the radial distribution patterns were more pronounced.
peaks and troughs was not observed. This was also true for the trees in Glindfeld (data not shown). Whereas the distribution patterns were stable in shape, concentration levels of Ni showed marked variations with the season. Highest Ni concentrations were often encountered in the samples collected in April (Table 2). April values were significantly higher than June values (P < 0.01 ) in two trees of Schwaney (nos. 1, 3) and in four trees of Glindfeld (nos. 1-4). The differences between the other months, i.e. June, September and December, were much smaller and rarely significant. In the
3.3. Seasonal variability of nickel distributions In order to investigate the stability of the described Ni patterns, the distributions were determined in the same trees in different months of 1 year (Figs. 1-5). The general patterns of Ni distribution in stem wood did not change considerably during the investigated period between April and December. Alterations in the radial Ni profiles were only of minor scale. A radial displacement of
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Year Fig. 5. Radial distribution o f Ni in stem wood o f beech tree No. 5 in Schwaney, Germany. For further details see Fig. 1.
J. Hagemeyer et al./Sci. Total Environ. 145 (1994) l l l - l l 8
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Year Fig. 6. Radial distribution of Ni in stem wood of 5 beech trees in Glindfeld, Germany. Data points represent means of 8 samples collected from the same tree at monthly intervals between April and December 1987. The small bars in each curve denote the center of the individual sapwood-heartwood transition. The broken vertical lines indicate the approximate range of the sapwood-heartwood transition zone for all trees which have a similar age.
tree Glindfeld 1, September values of Ni were significantly higher than December levels (P < 0.05) and in tree Glindfeld 5, June values were higher than those of December (P < 0.05). In two trees, no significant differences at all were found in the Ni levels of the four investigated months (Schwaney 2 and 4). 4. D i s c u s s i o n
Nickel concentrations in stem wood of beech trees from two sites in Germany showed distinct radial distribution patterns. Highest levels were observed in the middle part of the sapwood. The general shape of such radial distribution patterns was preserved during one vegetation period between April and December. However, the concentration levels, showed marked seasonal variations; highest Ni concentrations were generally found in samples collected before bud break, in April. During and after the vegetation period, Ni levels in stem wood were lower and more stable. The results indicate redistributions of Ni in stem wood of beech trees during the course of 1 year. Seasonal variations of various elements in xylem
sap of mature beech trees, e.g. Cd, Ca, Mg, K and Mn were reported by Glavac et al. (1990a,b). The observed concentration changes were apparently related to variations in the physiological status of the trees during the year. Highest levels of Cd, Ca and Mn were determined during the spring mobilization period in April. This agrees with our observation of highest Ni concentrations in the wood at the same time (Table 2). The presented Ni concentrations in wood, which were determined after wet ashing of the material, are total contents. They represent combinations of different fractions of the element, which occur in the xylem tissue. Part of the Ni is readily mobile in xylem sap. Another fraction is probably bound as Ni ions by electrostatic force to fixed negative charges in the xylem vessel walls. This was described for Ca, Cd and other cations as well (Ferguson and Bollard, 1976; Petit and Van de Geijn, 1978; McGrath and Robson, 1984). Binding to fixed negative charges is a reversible process. The Ni ions can be exchanged against other ions and become remobilized, whenever the ionic composition or the pH of the xylem sap have changed. This will occur in connection with physiological processes during the annual cycle of growth in deciduous plants (Ferguson et al., 1983). After their release, the ions are transferred in the xylem sap stream into other parts of the tree. A basipetal transport is possible in the phloem elements (Hill, 1980; Neumann and Charnel, 1986). Such circulation processes can explain the observed variations of Ni concentrations in the wood. The radial distributions of elements in stem wood were shown to depend in part on the cation exchange capacity of the tissue. In stem wood of Picea rubens, the density of fixed negative charges in cell walls varies on the radius of the stem (Momoshima and Bondietti, 1990). The highest charge density was observed in the stem center. The measured increase in Ca concentrations towards the stem center was attributed to the increased binding capacity of the wood. Also the Ni concentrations in beech wood showed higher values near the center of the stem (Figs. 1, 2, 4 and 5). It is not known, whether this is actually related to the cation binding capacity of the xylem. |t seems, however, likely, that the cation exchange
J. Hagemeyer et al./Sci. Total Environ. 145 (1994) 111-118
capacity of the wood tissue will affect the distribution of nickel. A pathway for radial transport of mineral elements within the stem are the rays. They consist of strands of living cells, extending radially through the xylem tissue. The movement of mineral nutrients in the rays was described by Ziegler (1968). Nutrients, like P, K and S are apparently transported towards the outer annual rings where they are used in living cells. Other elements, e.g. Ca, seem to be transported into the inner parts of the stem. Such processes can also influence the distribution of Ni in stem wood. The highest contents were found in the sapwood, close to the transition to heartwood (see Fig. 1). This distribution can be caused by a centripetal transport process in connection with heartwood formation. It was suggested, that the conversion of sapwood into heartwood is linked to a centripetal transport of physiologically useless waste substances in the rays (Stewart, 1966). The accumulation of toxic waste, including trace metals, can cause the death of ray cells and the formation of heartwood. Thus, the Ni peak in the older sapwood of beech trees may result from a centripetal transport of the toxic element towards the sapwood-heartwood transition. Here the ray cells are dying from a build-up of toxic material and the transport is interrupted. A similar mechanism was assumed to operate in oak trees (Quercus robur, Q. petraea), in which the highest concentrations of Cd were also found in the inner sapwood (Hagemeyer and Breckle, 1986). The hypothesis outlined suggests, that trees may even show an accelerated conversion of sapwood into heartwood under conditions of severe trace element pollution. An influence of the sapwood-heartwood transition on radial distribution patterns of elements in the trunks was described for a variety of tree species, including Fagus sylvatica (Hagemeyer et al., 1992), Fagus grandifolia (Brownridge, 1984), Quercusmongolica and Pinus koraiensis (Chun and Hui-yi, 1992) and Cryptomeria japonica (Okada et al., 1987). Physiological processes can obviously affect the distribution of elements in the wood of trees. This should be considered, when radial distribution patterns are used to monitor changes in environmental pollution levels in the past. A pattern, that
117
is influenced by radial element movements cannot be used to infer the extent of trace element pollution in former years. Apparently, the measured Ni concentrations in the wood are not stable during the time between deposition in the xylem and the analysis, years later. A year-to-year chronology of Ni pollution from analytical data of annual rings of beech seems, therefore, not feasible. In order to learn more about the factors governing the Ni distribution in tree stems, it will be useful to determine the sizes and relative quantities of the different fractions of Ni occurring in wood. Particularly the magnitude of the mobile fraction in relation to the total content can give an indication of the possible extent of Ni circulation in the tree. Data of the cation binding capacity of the wood will facilitate the interpretation of radial distribution patterns of Ni and other mineral elements. Furthermore, the question of the degree of radial mobility of Ni across annual growth rings should be tackled in future investigations.
5. Acknowledgments The investigation was partly funded by a grant of the Ministerium ffir Umwelt, Raumordnung und Landwirtschaft des Landes NRW, Dfisseldorf. Our thanks are extended to Katharina Lohrie for critical remarks on the manuscript.
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