AOBPreview originally published online on January 13, 2005
Annals of Botany 2005 95(4):661-672; doi:10.1093/aob/mci063
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Annals of Botany 95/4 © Annals of Botany Company 2005; all rights reserved
Differences in Growth Characteristics and Dynamics of Elements Absorbed in Seedlings of Three Spruce Species Raised on Serpentine Soil in Northern Japan
1 Hokkaido University Forests, FSC, Sapporo 060-0809, Japan and 2 Symbiotech Research Inc., Alberta, Canada T9E 7N5
* For correspondence. E-mail tkoike{at}exfor.agr.hokudai.ac.jp
Received: 6 July 2004 Returned for revision: 7 September 2004 Accepted: 16 October 2004 Published electronically: 13 January 2005
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ABSTRACT |
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 TOPFOOTNOTES ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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• Background and Aims Serpentine soils are characterized by the presence of heavy metals (Ni and Cr) and excess Mg; these elements often suppress plant growth. Picea glehnii is nevertheless distributed widely on serpentine soils in northern Japan. Growth characteristics were compared among P. glehnii, Picea jezoensis (distributed in the same region) and Picea abies (planted for timber production), and concentrations of elements in various tissues over time and the amount of ectomycorrhizal infection in short roots were evaluated.
• Methods Seedlings of three spruce species were planted in two types of experimental plots, comprising serpentine soil and brown forest (non-serpentine) soil, and these seedlings were grown for 3 years. Growth, ectomycorrhizal infection of short roots, and elemental composition of tissues were examined.
• Key Results The total dry mass of P. glehnii planted on serpentine soil was almost the same as on brown forest soil, and a large number of needles survived to reach later age classes. By contrast, growth of P. jezoensis and P. abies in serpentine soil was significantly less than in brown forest soil, and needle shedding was accelerated. Moreover, roots of seedlings of P. glehnii on serpentine soil were highly infected with ectomycorrhiza, and the concentration of Ni in needles and roots of P. glehnii was the lowest of the three species.
• Conclusions Picea glehnii has a high ability to maintain a low concentration of Ni, and the ectomycorrhizal infection may have the positive effect of excluding Ni. As a result, P. glehnii is more tolerant than the other spruce species to serpentine soil conditions.
Key words: Picea glehnii, Picea jezoensis, Picea abies, serpentine soil, growth, needle longevity, ectomycorrhiza, nutrient physiology, metal exclusion
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INTRODUCTION |
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TOPFOOTNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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The Sakhalin spruce (Picea glehnii) and Yezo spruce (Picea jezoensis) are the dominant coniferous species in the mesic region of northern Japan (Miyawaki, 1988
). Norway spruce (Picea abies) was introduced into Japan in the early 1900s for timber production, and is well adapted to mesic sites (Kubota and Fukuchi, 1981). Picea glehnii displays early successional characteristics (Sakagami and Fujimura, 1981) and can grow on serpentine soil and in infertile environments (Tatewaki, 1943, 1958; Matsuda, 1989). Picea jezoensis and P. abies are classified as late successional species, and usually grow on fertile soils (Miyawaki, 1988; Nikolov and Helmisaari, 1992). Also, P. jezoensis and P. abies are rarely found on serpentine soils (Tatewaki and Igarashi, 1971; Brooks, 1987).
Serpentine soils are formed by weathering of ultramafic rocks (Brooks, 1987). These soils are characterized by an excess of elements (such as Ni, Cr and Mg), a low Ca : Mg ratio, and low levels of several essential plant nutrients (Proctor, 1971; Brooks, 1987). Excess Ni has a negative effect on plasma membrane polarization, ion uptake and translocation, cell mitotic activity, and carbon partitioning in roots (Lee et al., 1978; Cocucci and Morgutti, 1986; Gabbrielli et al., 1990; Yang et al., 1996). Consequently, root growth is inhibited by the uptake of Ni (Jones and Hutchinson, 1986, 1988a; Dixon and Buschena, 1988; Jones et al., 1988; Yang et al., 1996; Tilstone and Macnair, 1997; Miller and Cumming, 2000). A high Mg concentration may lead to substitution of extracellular Ca by Mg via mass action, altering cell wall stability and plasma membrane permeability (Marschner, 1995). However, toxicity of serpentine soils for growth of P. glehnii has not been evaluated.
Some plant species are tolerant of edaphic factors in serpentine soils. Tolerance mechanisms of plants that adapt to high concentrations of heavy metals in soils can generally be summarized as either restricting metal uptake and translocation (exclusion) or accumulating the metal in a non-toxic form (accumulation) (Baker, 1981, 1987). In P. glehnii seedlings grown in serpentine soil, the concentration of Ni in needles was lower than in other species (Blandon et al., 1994; Kayama et al., 2002). Picea glehnii may therefore be a Ni excluder. Also, ectomycorrhizal symbiosis might play an important role in excluding toxic metals. Once the roots of woody species have been inoculated with ectomycorrhiza, the concentration of Ni in the leaves decreases, and root growth is accelerated despite the high concentration of Ni (Jones and Hutchinson, 1986, 1988a, b; Dixon and Buschena, 1988; Jones et al., 1988; Wilkins, 1991). Previous studies have examined only the growth characteristics and nutrient physiology of dominant serpentine species (Gabbrielli and Pandolfini, 1984; Gabbrielli et al., 1990; Miller and Cumming, 2000). It therefore remains unclear whether dominant serpentine species can exclude Ni and Mg through their intrinsic characteristics or whether this requires a high level of ectomycorrhizal symbiosis.
It was hypothesized that P. glehnii may have a high ability to exclude toxic metals, such as Ni and Mg, on serpentine habitats. Picea glehnii growing on serpentine soil may also have elevated ectomycorrhizal colonization compared with other spruce species. It would therefore be able to maintain growth even in serpentine conditions.
To test these hypotheses, ecophysiological traits of three spruce species, specifically (a) the growth characteristics of seedlings, (b) symbiosis of ectomycorrhiza on short roots, and (c) concentrations of elements in plant organs, were examined. The seedlings were grown in two types of nursery, prepared on a serpentine soil and on a brown forest (non-serpentine) soil, and the growth and elemental composition of the three spruce species were evaluated over 3 years.
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MATERIALS AND METHODS |
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TOPFOOTNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Study site
The experimental site was located in the Teshio Experimental Forest (TEF) of Hokkaido University (45°06'N, 142°12'E, 110 m a.s.l.). Serpentine soils are distributed in the eastern part of TEF, and P. glehnii is dominant in this region (Tatewaki and Igarashi, 1971
; Nakata and Kojima, 1987). The mean annual precipitation was approx. 1200 mm year–1. The annual mean, maximum and minimum temperatures were, respectively, 5·2 °C, 32·0 °C and –33·5 °C for the most recent 30 years, as measured by a thermorecorder at the Kami-toikan Meteorological Station (TEF, unpublished data). The distance between the meteorological station and the experimental site was approx. 7 km.
Experimental plot
Two experimental plots, one on a serpentine soil and one on brown forest soil were established. According to the FAO–UNESCO systems, serpentine and brown forest soils were classified as Podzol and Cambisol, respectively (Nakata and Kojima, 1987). The soil in each experimental plot was cultivated using a tractor to reduce soil heterogeneity. The size of a single seedling bed was 2 x 20 m and it was divided into two blocks. Four replications of the seedling bed were made in each plot. The distance between the two experimental plots was approx. 100 m.
Plant materials
To eliminate the difference in genetic characteristics caused by climatic and edaphic factors, seeds of P. glehnii Masters and P. jezoensis Carr. were selected from a similar habitat in the central part of Hokkaido, governed by the National Forestry Research Institute, where the soil was non-serpentine. About 100 years ago, P. abies (L.) Karst. was introduced from south-western Germany (Kubota and Fukuchi, 1981), and second generation seeds have been produced in the central parts of Hokkaido. Four-year-old seedlings of P. glehnii and P. jezoensis and 2-year-old seedlings of P. abies were used because of a shortage of equally aged seedlings. The seedlings were grown on clay loam soils (Cambisol) in the central part of Hokkaido before transplanting. One hundred and sixty seedlings of each spruce species were removed from the nursery in May 1999 and transported to the two experimental plots of TEF in early June 1999. During transportation, roots of each seedling were protected by moist paper towels (Kimtowel, Crecia Co., Tokyo, Japan). Eighty seedlings of each spruce species were planted in the experimental plots of serpentine and brown forest soils, respectively. After planting, each plot was weeded periodically. Water status was monitored by time domain reflectometry (TRIME-FM, IMKO Micromodultechnik GmbH, Ettlingen, Germany). The water content at field capacity of serpentine and brown forest soils was 48 %, and water was supplied if the water content fell below 35 %.
Analysis of soil chemistry
Soil properties, including pH and concentrations of carbon, nitrogen, exchangeable phosphorus, base cations and heavy metals, were measured. The soils in each experimental plot were sampled at a depth of 3 and 15 cm every month in each block to determine the soil pH and concentrations of elements. Almost no time variation between samples was found during the experimental period. Moreover, detailed soil chemistry was analysed in October 2000, and four samples of soils at depths of 3 and 15 cm were collected from four blocks in each plot. To determine the soil pH, 25 ml of distilled water was added to 10 g fresh soil to make a homogenized mixture (Van Reeuwijk, 1993). This soil mixture was then shaken for 1 h and the soil pH was measured using a pH meter (HM30V, TOA Electronics Ltd., Tokyo, Japan). Soil samples were also oven dried at 105 °C for 24 h prior to chemical analysis. The carbon and nitrogen contents of the dried soils were determined using a CHNS/O analyser (PE 2400 series II, Perkin-Elmer, Norwalk, CT, USA). Exchangeable phosphorus was separated using 0·5 N sodium bicarbonate (Olsen and Sommers, 1982), with shaking, for 1 h. Exchangeable base cations (Ca, Mg, K and Na) were obtained by mixing 2·5 g of dry soil with 50 ml of 1 N ammonium acetate solution, with shaking, for 1 h. Nickel was determined by the DTPA method (Baker and Amacher, 1982) and chromium by the nitric acid method (Reisenauer, 1982). Phosphorus, base cations and heavy metals in the extracted solutions were analysed by an inductivity coupled plasma analyser (IRIS, Jarrel Ash, Franklin, MA, USA). Also a standard solution of elements at interval of 20 samples was analysed, and the data compensated for accordingly.
Measurement of seedling growth
To determine the growth characteristics of seedlings of the three spruce species, the dry mass of needles, stems, and branches and roots was measured. Four seedlings of each spruce species planted on serpentine and brown forest soils were harvested in June 1999, May 2000, November 2000 and October 2001 (initial, 11th, 17th and 28th month harvest) from four blocks in each of the two nurseries. Roots of harvested seedlings were washed three times with water to remove soil, and finally by an ultrasonic washer (US-2A, As One Co., Osaka, Japan) with distilled water for 15 min. The washed seedlings were divided into shoot (organs above ground) and root components, and shoots were divided into components of each age. Each component was put into its own envelope and was oven-dried at 80 °C for 4 d. The dry masses of the various components were then determined.
To estimate needle longevity, the survival of needles (SN) was calculated at the 28th month harvest. The total needle dry mass and mass per needle were weighed for needles of each age at the four harvest periods, and the SN was calculated as follows (Kayama, 2002):
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Measurement of the rate of infection of ectomycorrhiza
To measure the proportion of roots with ectomycorrhizal infection, ten lateral roots were randomly selected from each seedling and then over 500 short roots (viz. <5 cm in length) that had emerged from them.
This proportion was determined before drying 16 seedlings of the three spruce species grown on the serpentine and brown forest soils. For assessment of ectomycorrhiza, roots of seedlings were harvested in the 1st, 17th and 28th months, and were carefully washed free of soil under gently flowing water. The root systems were observed under a stereomicroscope, and the numbers of infected and uninfected short roots counted (Quoreshi and Timmer, 1998). The percentage of short roots infected by ectomycorrhiza was then calculated.
Analysis of nutrition in plants
Concentrations of N, P, K, Ca, Mg and Ni in 2-year-old needles, stems and roots were determined. Two-year-old needles were used because it takes 2 years for new needles to reach their maximum physiological activity (Hom and Oechel, 1983). The dried samples were ground to a fine powder using a vibrating sample mill (TI-100; Tester Industry Co., Tokyo, Japan). The concentration of N was determined using a CHNS/O analyser (PE 2400 series II, Perkin-Elmer, Norwalk, CT, USA). To determine the concentration of the other elements (P, K, Ca, Mg and Ni) dried samples were digested in the microwave digestion system (O·I Analytical, College Station, TX, USA) and analysed using an inductivity coupled plasma analyser. A standard solution of each element was also analysed at an interval of 20 samples to ensure the analysis was reliable. Mg and Ni were also analysed in various age classes of needles and in part of the roots at the 28th month harvest.
Roots of seedlings of the three spruce species planted on serpentine soil were separated using a sieve of mesh diameter 2·0 mm, and categorized into thin roots (<2·0 mm diameter) and thick roots (>2·0 mm diameter) at the 28th month harvest. Thin and thick roots were digested separately, and were analysed for N, P, K, Ca, Mg and Ni.
Statistical analysis
Stat View 5·0 (SAS Institute Inc.) was used for statistical analysis of all parameters. The mean dry mass of each organ, survival of needles, percentage infected by ectomycorrhiza, and concentrations of elements in needles, stems and roots, were all examined using t-tests. The mean values were compared for the three spruce species between the serpentine and brown forest soils. For analysis of soil chemical properties, depth and soil type were tested by repeated measures of ANOVA.
The mean values of the concentrations of elements in Figs 5 and 6 were examined using the Tukey test. From Fig. 5, the mean values for needles of the three spruces were compared at each age, and in Fig. 6 the mean values for the two types of roots of the three spruces were compared.
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All mean values of four blocks of experimental plots were also examined by a single ANOVA, and there were no significant differences among four blocks.
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RESULTS |
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TOPFOOTNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Soil chemical properties
Table 1 lists chemical properties of the two soils. Serpentine soil had a higher pH (6·7) than brown forest soil (5·2; P < 0·001). Concentrations of Mg, K, Na, Ni and Cr were higher in serpentine soil than in brown forest soil (P < 0·001). By contrast, the concentrations of C and N were higher in brown forest soil than in serpentine soil (P < 0·05). Concentrations of P and Ca did not differ significantly between serpentine soil and brown forest soil. The concentrations of C, N, P and Ca were significantly lower in samples taken at a depth of 15 cm than at 3 cm (P < 0·05). There was a significant interaction in concentration of P between soil depth and soil types (P < 0·001).
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Growth characteristics
The dry masses of each organ of P. glehnii did not differ significantly between the two soils, except for the needle dry mass in the 28th month (Fig. 1). By contrast, the dry masses of each organ of P. abies on serpentine soil were smaller than those from brown forest soils (P < 0·05). Picea abies growing on brown forest soil underwent markedly large growth in 2001, such that the dry mass of each organ rose to three times greater than for seedlings on serpentine soil. For P. jezoensis, the needle dry mass on serpentine soil was smaller than on brown forest soil after the 11th month (P < 0·05). The root dry mass for P. jezoensis grown on serpentine soil was also significantly smaller than on brown forest soil at the 11th and 17th months.
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Survival of needles (SN) of the three spruce species was reduced by ageing of the needles, especially in P. jezoensis (Fig. 2). The SN for P. glehnii on serpentine soil was higher for 2-year-old needles than on brown forest soil (P < 0·05). By contrast, the SN for P. jezoensis and P. abies on serpentine soil was lower than on brown forest soil for needles 2 years of age and older (P < 0·05).
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Percentage of ectomycorrhizal infection
At the initial harvest, the ectomycorrhizal infection percentages for shoot root of P. glehnii, P. jezoensis and P. abies were, respectively, 32·6, 33·3 and 41·6. Ectomycorrhizal development on the three spruces had not changed by the 11th month harvest (data not shown). By the 17th month, the ectomycorrhizal infection percentage of the three spruces had increased, reaching approx. 60 % for P. glehnii and P. jezoensis on brown forest soil (Fig. 3). Colonization of P. glehnii on serpentine soil was 80 % (P < 0·001), whereas P. jezoensis had declined to 40 % (P < 0·001). For P. abies the colonization percentage was about 80 %, and there was no significant difference between the two types of soil.
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By the 28th month, all of the spruce species grown on brown forest soil had increased ectomycorrhizal colonization levels. On serpentine soil, P. jezoensis had increased colonization levels, whereas those of P. glehnii and P. abies were nearly the same at 17 and 28 months. For P. jezoensis and P. abies on serpentine soil, ectomycorrhizal colonization was lower than on brown forest soil (P < 0·001); for P. glehnii there was no significant difference.
Element concentrations
Concentrations of elements in 2-year-old needles, stems and roots are shown in Tables 2, 3 and 4, respectively. The N concentration in needles, stems and roots of the three spruces was lower on serpentine soil than on brown forest soil from the 11th month onward (P < 0·05). In particular, the N concentration in needles of the three spruces grown on serpentine soil was half the value found in spruces grown on brown forest soil.
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At the 28th month harvest, the P concentrations in needles and stems of the three spruce species grown on serpentine soil were lower than in those grown on brown forest soil(P < 0·01). For the P concentration in the roots of P. glehnii, there was no significant difference between serpentine and brown forest soils at any harvest. By contrast, the concentration of P in roots of P. jezoensis and P. abies on serpentine soil was lower than for specimens grown on brown forest soil (P < 0·01).
The concentrations of K in stems and roots of the three spruce species grown on serpentine soil were lower than in seedlings grown on brown forest soil at the 28th month harvest (P < 0·01). For needles at the 28th month harvest, the K concentration was significantly higher in P. glehnii grown on serpentine soil than on brown forest soil.
The Ca concentrations in needles of the three spruce species grown on serpentine soil were lower than those in plants on brown forest soil at the 28th month harvest (P < 0·001). Regarding Ca in the roots, P. glehnii and P. abies grown on serpentine soil had higher concentrations than those in plants grown on brown forest soil, from the 11th month harvest onwards (P < 0·05).
Marked differences were observed in concentrations of Mg and Ni in each organ of the three spruce species. Concentrations of Mg and Ni were higher on serpentine soil than on brown forest soil from the 11th month harvest onwards (P < 0·001).
The concentrations of Mg and Ni in needles of plants grown on serpentine soil were found to increase with needle age (Fig. 4). Of the three spruce species, concentrations of Mg and Ni were highest for P. abies (P < 0·05). The concentrations of Mg and Ni in P. glehnii were always lower than in P. abies and in the oldest needles were also lower than in P. jezoensis. For P. jezoensis, the pattern of accumulation of Mg in needles was similar to that in P. glehnii, although the pattern of accumulation of Ni in P. jezoensis was similar to that in P. abies.
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Concentrations of Mg and Ni for each spruce were significantly higher in thin roots than in thick roots (Fig. 5, P < 0·01). The Mg and Ni concentrations in thin roots of P. glehnii grown on serpentine soil were lower than in these roots for the other spruce species (P < 0·05). In particular, the Ni concentration in thin roots of P. glehnii growing on serpentine soil was 3·5 µmol g–1 d. mass, the lowest value of the three spruces.
To determine the total accumulation and transport of toxic elements, the total content of Mg and Ni was calculated in each organ of the three spruce species grown on serpentine soil (Fig. 6). The total content of Mg and Ni in P. glehnii and P. jezoensis increased drastically at the 11th month harvest, and accumulated in the above-ground organs. At the 17th month harvest, the amount of Mg and Ni in above-ground organs of P. glehnii and P. jezoensis had fallen, and these elements had accumulated in roots. By contrast, the total content of Mg and Ni in P. abies grown on serpentine soil gradually increased during the experimental period.
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DISCUSSION |
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TOPFOOTNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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The maintenance of growth, tissue nutrient concentrations, and limited Ni accumulation exhibited by P. glehnii seedlings suggest that this species is adapted to serpentine soil conditions (Fig. 1). The superior performance of P. glehnii on serpentine soil may be the result of specific physiological mechanisms limiting Mg and Ni uptake (Gabbrielli et al., 1990
) or may be affected by symbiotic ectomycorrhizal fungi (Jones and Hutchinson, 1988b; Jones et al., 1988). The concentration of Ni in needles of P. glehnii on serpentine soil at the 28th month harvest was lower than in the other spruces (Table 2 and Fig. 4). Toxic elements of P. glehnii grown on serpentine soil accumulated in roots from 17th month onwards (Fig. 6). Picea glehnii may therefore be able to inhibit transportation of Ni to its needles, with retention of Ni in thin roots (Fig. 5). Consequently, P. glehnii may be able to increase its growth and maintain a high survival of needles irrespective of the high concentrations of Ni and Mg in serpentine soil.
By contrast, seedlings of P. jezoensis and P. abies grown on serpentine soil showed significant decreases in dry masses of each organ (Fig. 1). Concentration of Ni in needles of P. jezoensis and P. abies on serpentine was higher than that of P. glehnii. Toxicity of Ni decreases photosynthetic capacity (Carlson, 1975; Jones and Hutchinson, 1988a; Yang et al., 1996; Kayama, 2002). It seems that P. jezoensis and P. abies grown on serpentine soil may suffer decreased photosynthetic production because of Ni toxicity; as a result, their growth is suppressed (Kayama et al., 2002). Moreover, P. jezoensis and P. abies had higher concentrations of Mg and Ni in their roots, especially in thin roots, than P. glehnii (Table 4 and Fig. 5). Ectomycorrhizal infection levels differ between P. jezoensis and P. abies, however (Fig. 3). It therefore seems that there are differing reasons (e.g. infection level of ectomycorrhiza or trait of absorption of toxic metals) for the high root concentrations of Mg and Ni in P. jezoensis and P. abies grown on serpentine soil. In P. jezoensis, the percentage of ectomycorrhizal short roots on serpentine soil was lower than for the other spruce species (Fig. 3). It appears that roots with no ectomycorrhizal association may have absorbed Mg and Ni, so that concentrations of Mg and Ni increased in roots of P. jezoensis on serpentine soil. Previous studies have found high concentrations of Ni in roots of non-ectomycorrhizal seedlings (Jones and Hutchinson, 1986, 1988a; Dixon and Buschena, 1988; Jones et al., 1988). Moreover, the needle dry mass of P. jezoensis fell at the 11th month harvest (Fig. 1). In this harvest, the concentration of Mg and Ni increased six-fold in needles of P. jezoensis in serpentine soil; this species shed its needles more quickly because of the toxicity of these elements. However, concentrations of Mg and Ni in needles of P. jezoensis on serpentine soil were almost the same as for P. glehnii. Needles of P. jezoensis may therefore be more sensitive to toxic elements than needles of P. glehnii.
The percentage of ectomycorrhizal short roots of P. abies on serpentine soil was 80 %, almost the same as for P. glehnii (Fig. 3). Ectomycorrhizal fungi in the roots generally increase the acquisition of P and N from the soil by the host plant (Marschner, 1995; Smith and Read, 1997). Picea abies on serpentine soil had high N accumulation, so that concentrations of N in needles were the highest of the three spruce species (Table 2). However, uptake of toxic elements by P. abies on serpentine soil was not inhibited in spite of the high amount of ectomycorrhizal infection (Fig. 6). It has been reported that P. abies has high sensitivity to various toxic metals including Pb, Cd, Hg and Zn (Galli et al., 1993; Godbold and Hüttermann, 1985; Marschner et al., 1996; Jentschke et al., 1999). Moreover, uptake of heavy metals by P. abies was not inhibited by inoculation of ectomycorrhiza (Jentschke et al., 1999). The present study suggests that a high amount of ectomycorrhizal infection did not assist P. abies to exclude Ni.
The present results show that concentrations of N, P and Ca in needles were lower in the three spruce seedlings grown on serpentine soil than those on brown forest soil. Critical values of deficiency or toxicity of each element are given in Table 5 and the concentrations of elements in 2-year-old needles of the three spruces planted on serpentine soil for 28 months were examined (Tables 2 and 5). N deficiency was found in P. glehnii and P. jezoensis, and P deficiency was detected in P. glehnii and P. abies. The concentration of Ca in needles of three spruces grown on serpentine was below 100 µmol g–1, and they could be regarded as Ca deficient. Previous studies found that, when plants are grown on serpentine soil, Ca uptake is often inhibited and the plants show Ca deficiency above a soil pH of 6·5 (Mizuno, 1979; Mizuno and Nosaka, 1992). In addition, the Ca : Mg ratio was examined for 2-year-old needles of three spruces. The Ca : Mg ratios of P. glehnii, P. jezoensis and P. abies at the 28th month were 0·71, 0·65 and 0·26, respectively. In general, a Ca : Mg ratio below 0·5 for Ca-deficient plants grown on serpentine soil is regarded as detrimental (Mizuno, 1979). The present results suggest that P. abies grown on serpentine soil is seriously Ca deficient because of excess Mg. Moreover, P. jezoensis suffered Mg toxicity, and P. jezoensis and P. abies suffered Ni toxicity. Also, P. abies grown on serpentine soil suffered Ni toxicity. It appears that Cr in the serpentine soil in this region forms a stable compound, which has quite a low solubility in water (Mizuno, 1979). It therefore seems that effect of Cr toxicity may also be low.
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Compared with other Pinaceae species grown on serpentine soil, concentrations of Ni and Mg in needles of three spruce seedlings were in a similar range (Kruckeberg, 1992
; Roberts, 1992). However, concentrations of Ni and Mg in needles were lower for 60-year-old P. glehnii, P. jezoensis and P. abies planted on serpentine soil in TEF (Kayama et al., 2002) than those of seedlings of the three spruces. Habitats were compared between the 60-year-old spruce plantation and the experimental plots. The distance between the two sites was approx. 15 km. The concentration of calcium in the soil of the experimental plots on serpentine soil (mean 25 mg 100 g–1) was quite a bit lower than that of the spruce plantation (mean 83 mg 100 g–1). Calcium ameliorates the toxicity of Ni and Mg (Brooks, 1987). When calcium was added to serpentine soil, the availability of Ni and Mg for plants decreased (Chiarucci et al., 1998), and the concentration of Ni and Mg in leaves also decreased (Mizuno, 1979; Brooks, 1987). This suggests that Ni and Mg toxicities are probably higher for experimental plots than those for the spruce plantation. Consequently, large amounts of Ni and Mg were absorbed by the three spruce seedlings planted on the experimental plots. Moreover, the decline in the survival of needles was faster for the three spruce seedlings on serpentine soil than for these species when mature. It seems that Mg and Ni toxicity could accelerate the death of needles on seedlings grown on serpentine.
Finally, it was concluded that the ability of P. glehnii to maintain a low concentration of Ni is good and, compared with P. abies, this species may benefit from the positive effect of ectomycorrhizal infection causing Ni to be excluded. Picea glehnii grown on serpentine soil maintained an adequate level of ectomycorrhizal infection without inoculation, reflecting the inherent characteristics of this species. Consequently, P. glehnii can survive and grow in various infertile environments (Tatewaki, 1943, 1958; Matsuda, 1989). Previous studies have also suggested that ectomycorrhizal association is important for excluding metals, but the role of ectomycorrhizal infection has not been studied in species adapted to serpentine (Brooks, 1987; Miller and Cumming, 2000). It was found that P. glehnii is more tolerant than the other spruce species to serpentine soil conditions.
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ACKNOWLEDGEMENTS |
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TOPFOOTNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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We thank Prof. M. Osaki, Dr Y. Matsuura, Dr Y. Akibayashi, Prof. K. Sasa and Prof. F. Satoh for their valuable comments on this study. We also thank Dr T. D. Colmer and two anonymous reviewers for their invaluable comments on the manuscript. We are grateful to the technical staff of Teshio Experimental Forest, Hokkaido University, for their excellent technical assistance. Thanks are also due to Dr S. Kitaoka and Ms Y. Yanagihara for preparation of the nurseries. Financial support given to M.K. and T.K. by JSPS and the Japan Science Society is gratefully acknowledged.
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FOOTNOTES |
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TOPFOOTNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Present address: JSPS Research Fellow, Hokkaido Research Center, Forestry and Forest Products Research Institute, Hitsujigaoka 7, Toyohira, Sapporo 062-8516, Japan. 
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LITERATURE CITED |
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TOPFOOTNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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