Plant Foods for Human Nutrition 58: 93–115, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.
Nutritional characteristics of the leaves of native plants growing in adverse soils of humid tropical lowlands MITSURU OSAKI1, TOSHIHIRO WATANABE1, TETSUYA ISHIZAWA1, CHAIRATNA NILNOND2, TANIT NUYIM3 , TAKURO SHINANO1, MASARU URAYAMA1 and SEHAT JAYA TUAH1
1 Graduate School of Agriculture, Hokkaido University, Kita 9, Nishi 9, Kitaku, Sapporo, 060-8589 Japan; 2 Faculty of Natural Resources, Prince of Songkla University, Hat Yai, 90110 Thailand; 3 Princes Sirindhorn Peat Swamp Forest Research and Nature Study Center,
Amphur Sungai Kolok, Narathiwat 96120, Thailand Received 16 March 2000; accepted in revised form 11 August 2000
Abstract. Acid sulfate, peat, sandy podzolic, and saline soils are widely distributed in the lowlands of Thailand and Malaysia. The nutrient concentrations in the leaves of plants grown in these type of soils were studied with the aim of developing a nutritional strategy for adapting to such problem soils. In sago and oil palms that were well-adapted to peat soil, the N, P, and K concentrations were the same in the mature leaves, while the Ca, Mg, Na, and Fe concentrations were higher in the mature leaves of the oil palm than of the sago palm. Melastoma malabathricum and Melaleuca cajuputi plants that were well-adapted to low pH soils, peat, and acid sulfate soils were also studied. It was observed that a high amount of Al accumulated in the M. marabathricum leaves, while Al did not accumulate in M. cajuputi leaves. M. cajuputi plants accumulated large amounts of Na in their leaves or stems regardless of the exchangeable Na concentration in the soil, while M. malabathricum that was growing in saline-affected soils excluded Na. Positive relationships between macronutrients were recognized between P and N, between K and N, and between P and K. Al showed antagonistic relationships with P, K, Ca, Mg, Fe, Zn, Cu, and Na. Na also showed antagonistic relationships with P, K, Zn, Mn, Cu, and Al. Fe showed weak antagonistic relationships with Zn, Mn, Cu, and Al. Key words: Acid sulfate soil, Al accumulator, Na accumulator, Palm, Peat soil, Saline soil, Sandy podzolic soil
Introduction Various adverse soils, such as peat, acid sulfate, sandy podzolic, and saline soils, are present in the tropical lowlands of southeast Asia. These soil properties vary widely among different soil types. When field crops are cultivated in or introduced into these adverse soils, they will suffer from serious nutritional problems. Nevertheless, some native plants grow well under these adverse
94 soil conditions, and it is important to discern how these plants manage to develop mechanisms for adaptation or tolerance. Aluminum (Al) toxicity is considered to be a serious problem in low pH soils [1]. Al toxicity is not characterized by a single effect, but can be complicated by various factors. One of the most important effects of Al on plant growth is in nutrient uptake. An inhibition of nutrient uptake caused by Al has been reported for several essential elements, including P [2], K [3], Ca [4, 5], Mg [6], Fe [7], Mn [8], Cu [9], and Zn [10]. The uptake of these elements was effected both directly, through antagonistic inhibition or precipitation, and indirectly, through phenomena such as disordering of membrane functions. Plant growth is also restricted by saline conditions, especially in the arid, semiarid and coastal regions where excessive Na is a problem. Salt toxicity in plants may cause (1) an inhibition of water uptake, (2) disorders in plant metabolism that result from high Na content in tissues [11], and (3) antagonistic relationships between Na uptake and K, Ca, and Mg uptake [11, 12]. The growth of some plant species that have adapted to low pH soils or saline soils is known to be enhanced by the application of Al [13, 14] and Na [15, 16], respectively. It can therefore be concluded that Al and Na are beneficial elements for these plant species. In these plant species, Al or Na accumulator plants can be found, whereas in most species, including general crops, plant shoots accumulate only very small amounts of Al or Na. Al accumulator plants are known to exist in the Melastoma malabathricum [13, 17], Miconia albicans [18], Vochysia thyrsoidea [19], Graffenrieda latifolia [20], and Tea [19] species. Na accumulator plants are known to exist in the Atriplex gmelini [16], Halogeton glomeratus [14], and Suaeda maritma [22] species. Since low pH soil-adapted plants, not only Al accumulator plants, grow well under the application of Al, it can be concluded that Al is not always a toxic ion for plants, but can stimulate plant growth or ion uptake [13, 14]. This research elucidated the general nutritional characteristics of the leaves (and sometimes stems) of various plant species that grow naturally in various adverse soils. Leaves of various plant species were therefore collected from several areas in the lowlands of Thailand and Malaysia, and their minerals concentrations were analyzed.
Materials and methods Sample collection and preparation Plants were sampled from fields distributed throughout Thailand and Malaysia that were made up of various adverse soils (Figure 1). Five to 10 fully expanded mature leaves (or shoots) of various species of grasses and trees,
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Figure 1. Sampling sites distributed in Thailand and Malaysia. Table 1. Chemical properties of peat, acid sulfate, and sandy podzolic soils.
96 Table 2. Mineral concentration in leaves in of palm grown in Thailand and Malaysia
excluding seedlings, were collected from each of the 5 to 10 plants sampled per field. The leaves (or shoots) were washed with deionized water, dried in an forced-air oven at 80 ◦ C, and ground. Soils (about 10 cm in depth) were collected from at least 5 locales in each field, then were mixed in the field and dried at room temperature. Dried soils were ground and passed through a 2-mm sieve. Soil pH (1:2.5 = soil : deionized water, shown in Tables 2, 3, 4, 5, 6, and 7) was measured in the field using a portable pH meter (Horiba).
97 Table 3. Mineral concentration in leaves, shoots and stems of plants grown in acid sulfate soils at Munoh, Pikultong center, Amphoe Pak Phayyun, and Toplama in Thailand
98 Table 4. Mineral concentrations in leaves and stems of plants grown on peat soils at Bacho, Kab Daeng, To Daeng, and Ban Pa Wai in Thailand.
99 .
Chemical analyses Nitrogen (N) concentration in the plant tissues was determined by the semimicro Kjeldahl method after the tissue was oxidized and decomposed using a mixture of sulfuric acid with salt (K2 SO4:CuSO4 = 5:1). Phosphorous (P) concentration was determined by the vanado molybdate yellow method, while potassium (K) and sodium (Na) concentrations were determined by flame photometry, and calcium (Ca), magnesium (Mg), iron (Fe), manganese (Mn),
100 Table 5. Mineral concentrations in leaves and shoots of plants grown in sandy podzolic soil at Bacho in Thailand
zinc (Zn), copper (Cu), and aluminum (Al) concentrations were determined by atomic absorption spectrophotometry after wet ashing with an acid mixture. Exchangeable K, Mg, Ca, and Na in the soils was extracted with 1N KCl (soil: KCl = 1: 20), and their concentrations were determined by flame photometry (K and Na) and by atomic absorption spectrophotometry (Ca and Mg). The amount of available P in the soils was determined by the Bray II method. Exchangeable H+ and Al in the soils was extracted as follows: 1) 4 g of soil was extracted with 10 ml of 1 N KCl over 30 min, 2) the extract was filtered once (Advantec Toyo No. 6 filter paper) and washed with 10 ml
101 Table 6. Mineral concentrations in leaves, shoots, and stems of plants grown in saline soils in Thailand
102 Table 7. Mineral concentrations in leaves and stems of plants grown on acid sulfate soils at Kuala Linggi in Malaysia
of 1 N KCl three times, and 3) steps 1 and 2 were each repeated three times. Amount of exchangeable H+ was determined by titration of aliquot of 0.1 N NaOH after the addition of phenolphthalein, and amount of exchangeable Al was determined by titration of aliquot of 0.1 N HCl after the addition of 2 mL of 4% NaF.
Statistical analysis Statistical analyses were carried out using the SPSS program (SPSS Inc., Chicago). Regressions were tested by the linear model: y = ax+b or the antagonistic model: y = c(d+x)/x, where a, b, c, and d are constants.
103 Results and discussion Soil property The pH (H2 O) of the acid sulfate, peat, and sandy podzolic soils fell respectively in the ranges of 3.2–4.4, 3.5–4.9, and 4.8 (Table 1). The pH (KCl) was lower in all soils than the pH (H2 O). The amount of available P (Bray II P2 O5 ) was small, especially in Toplama (acid sulfate), Bacho (sandy podzolic), and Kuala Lingi (acid sulfate in field). Exchangeable cations (Ca, Mg, K, and Na) had a tendency to be high in peat soil and quite low in acid sulfate soils and sandy podzolic soil. In the sandy podzolic soil, the amount of exchangeable K was extremely low. The exchangeable Al concentration was high in Munoh (acid sulfate soils) and low in peat soils. Mineral concentrations in the leaves of palm trees In sago palms grown in various locations, the macronutrient concentration (g/kg) in mature leaves varied within the ranges of 10.4 to 20.6 for N, 0.5 to 1.4 for P, 2.7 to 10.3 for K, 1.7 to 3.4 for Ca, and 0.6 to 1.4 for Mg, and the micronutrient concentration (mg/kg) varied within the ranges of 12 to 56 for Na, 34 to 530 for Mn, 31 to 153 for Fe, 13 to 39 for Zn, 1 to 32 for Cu, and 0 to 215 for Al and 11 to 153 for B (Table 2). Accordingly, the N, P, K, Ca, Mg, and Na concentration in leaves varied slightly regardless of soil type. Also, the K concentration in leaves grown in peat soil was not affected by the potassium application (6 g/m year). In peat soil, it is difficult to cultivate maize, tomatoes [24], barley, or rice [25] because of the low pH, poor nutrients, and the toxicity of phenolic compounds. On the other hand, sago palms can grow in peat soil with no fertilizer application [26]. Also, sago palms have a tolerance to poor nutrient conditions because their growth mechanism is active even when the nutrient concentration in their leaves is low compared to that of field crops. The oil palm is not native to this area, but it was observed growing in various adverse soils. The macronutrient concentration (g/kg) of mature leaves from oil palms found growing in various locations ranged from 16 to 17 for N, 1.1 to 1.4 for P, 2.3 to 5.6 for K, 8.0 to 11.7 for Ca, and 2.2 to 8.7 for Mg, while the micronutrient concentrations (mg/kg) ranged from 46 to 1091 for Na, 29 to 654 for Mn, 67 to 310 for Fe, 11 to 65 for Zn, 7 to 42 for Cu, and 67 to 320 for Al and 78 for B (Table 2). In oil palms from other parts of the world, the nutrient concentrations (g/kg) in the leaves have ranged from 16.8 to 28.2 for N, from 1.1 to 2.0 for P, and from 6.7 to 18.7 for K. Note that the lower values in these ranges were estimated from deficiency treatments. Oil palms were grown with annual grasses because annual crops absorb large amounts of minerals [27]. The critical concentrations (g/kg) of
104 macronutrients, i.e., the concentration that gives the maximum yield, in the 9th leaf of younger oil palms were found to be 27.5 for N, 1.6 for P, 12.5 for K, 6.0 for Ca, and 2.4 for Mg [28]. Thus, since the N and K concentrations in oil palms grown in Narathiwat peat soil were below the critical levels, N and K must limit the growth of oil palms. The optimum concentrations (mg/kg) of micronutrients in the leaves of oil palms were found to be 200 for Mn, 100 to 200 for Fe, 15 to 20 for Zn, and 5 to 7 for Cu [29]. Ng & Tan [30] reported that leaf chlorosis and poor leaf growth, seen as a symptom of peat yellow, was observed as a result of K and Cu deficiencies in which the K concentration (g/kg) and Cu concentration (mg/kg) were 10.9 and 1.6, respectively. It should be noted that the K concentration was lower in the peat soil of Thailand than in the peat soil of Malaysia, but chlorosis was not observed in the oil palms grown in peat soil in Thailand. In the tropical peat soils distributed in the lowlands of Thailand and Malaysia, low pH and low K levels were the most important factors limiting crop growth, followed by low P and low N levels [31]. However, few differences were observed in the mineral concentrations in the leaves of sago and oil palms grown both in peat soil and mineral soil. N, P, and K concentrations were not significantly different between the two types of palms, but the Ca, Mg, Na, and Fe concentrations in the mature leaves were higher in the oil palm than in the sago palm (Table 2). Cu and B concentrations in the leaves were quite low in the palms grown in peat soil, with the Cu deficiency being especially marked, and considered the most important among the micro nutrient deficiencies in the peat soils of Thailand and Malaysia [31]. The Cu sufficiency range in the leaves of various plants is between 3 and 7 mg/kg Cu [32]. Peat soil is therefore Cu-deficient (Table 2). B requirements can be separated into three groups: the required leaf concentration in the monocot, which is 1 to 6 mg/kg, that in the dicot, which is 20 to 70 mg/kg, and that in the dicot with a latex system, which is 80 to 100 mg/kg [32]. As sago and oil palms are monocot, they are presumably not highly deficient in B. Mn, Fe, and Zn concentrations varied among locations (Table 2), however it is assumed that they fall within the normal range because the concentration ranges for leaf sufficiency are 15 to 50 mg/kg for Zn, 10 to 50 mg/kg for Mn, and 50 to 75 mg/kg for Fe [32]. The Nipa palm (Nipa fruticans) is the mangrove palm, which is found in belts or in extensive blocks along river edges. The Na concentration in the leaves of the Nipa palm was 1376 to 6151 mg/kg (Table 2). Sago palms are often integrated with mixed Nipa palms, although the Na concentration in the leaves of the Sago palm is less than 100 mg/kg (Table 2). Since the saline tolerance is stronger in the Nipa palm than in the Sago palm, Na concentration in the leaves can be taken to be one indicator of Na tolerance.
105 Mineral concentrations in leaves or stems of native plants growing in various adverse soils Mineral concentrations in plants growing in acid sulfate soils. In acid sulfate soils adjacent to peat soils in Thailand and Malaysia, Melastoma sp. and Melaleuca sp. are the dominant shrubs and trees, respectively, and Scleria sp., Cyperus sp., and Paspalum sp. are the main grasses. The Al concentration in the leaves and stems of Melastoma sp. and Cyperus haspen was extremely high, while that of Melaleuca sp. was negligible (Tables 3 and 7). Chenery [33], and Chenery & Sporne [34] defined plants as Al accumulators when the shoot (mainly the leaf) accumulates Al at a concentration greater than 1000 mg/kg. Therefore, Melastoma sp. and C. haspan are defined as Al accumulator plants. Melastomataceae are well adapted to low pH soils and are well documented to be Al accumulator plants. They have been shown to have accumulated Al in the following concentrations: 1350–5796 mg/kg [35], 9600–11000 mg/kg [36], and 4310–6630 mg/kg [19] in Central Brazil and 6899 mg kg−1 in the Orinoco Llanos of Venezuela. In this paper, M. cajuputi, Paspalum conjugatum, Xyris indica, and Scleria sumatrens are defined as Al excluder plants because the Al concentration in the leaves of these species is less than 100 mg/kg (Table 3) in spite of the high exchangeable Al content in the soil (Table 1). Although the concentration of exchangeable Na in acid sulfate soils was not found to be high (Table 1), Melaleuca sp., P. repens, C. haspan, Ischaemum aristatum, Ischaemum barbatum, and Olax scandens were seen to accumulate large amounts of Na in their leaves or stems (Tables 3 and 7). M. cajuputi, P. repens, and C. haspan can also be grown in saline affected soil or saline soil (Tables 3 and 6, and observation). Thus, some species can survive under conditions of extremely low pH and high salinity (Table 3). Many of these species, such as M. cajuputi, Flagellaria indica, Acrostichum aureun, Dalbergia nigrescens, and Acanthus ebracteatus accumulate large amounts of Na in their leaves, while M. malabathricum does not accumulate Na even if the Na concentration in the soil is high. Little is known about the toxicity of Mn in acid sulfate soils. Soil that is rich in Mn and has a low pH tends to produce Mn toxicity, particularly under alternately wet and dry conditions [37]. The leaf sufficiency concentration of Mn ranges from 10 to 50 mg/kg in the dry matter of mature leaves, and Mn toxicity symptoms will develop when the Mn concentration reaches levels higher than 600 mg/kg in soybeans, 700 mg/kg in cotton, and 1380 mg/kg in sweet potatoes [32]. Since the Mn concentration observed in the samples in this study was in all cases less than 617 mg/kg, Mn toxicity might not appear in native plants (Tables 3 and 7).
106 Mineral concentrations in plants growing in peat soils. Because the concentration of exchangeable Al in peat soils is quite low (Table 1), the Al concentration in the leaves of most species grown in these soils is not high (Table 4). M. malabathricum, however, accumulates relatively high Al in its leaves, indicating that M. malabathricum accumulates Al actively. Also, although the level of exchangeable Na is quite low in peat soils (Table 1), some plants, such as M. cajuputi, C. haspen, Xyres complanata, and Paspalum logifolium, still accumulate Na actively (Table 4). Generally, it is assumed that Na accumulates in plant tissues as a result of high Na concentrations in soils. However, some plants grown in peat soil as well as acid sulfate soil accumulate Na actively in spite of the low concentration of exchangeable Na in the soil. Studying the salt accumulation mechanisms in these plants may provide very important insight into how plants have acquired the salt tolerance necessary to thrive in high saline soils. Of particular interest is the lack in these peat soils of some micronutrients, which may become a nutritional factor limiting crop growth. Several researchers have observed Cu deficiencies in maize [38, 39], sorghum and groundnuts [40], and pineapples [41], B deficiencies in tomatoes [42], and deficiencies of Cu, B, Zn, and Mn in oilpalm [30]. However, information is still lacking on the effect of soil pH on the availability of micronutrients in tropical woody peat soils, and on the optimum pH for crop growth in relation to the availability of micronutrients. On the other hand, sterility becomes a serious problem in peat soils when rice plants are cultivated. The presence of a copper deficiency, the toxicity of phenolic compounds, or the combined effect of both of these factors have been cited as the causes of the sterility that occurs when plants suffer from deficiencies in Cu [43] and B [44]. The Cu concentations in the leaves of plants grown in peat soils were quite low compared to those in plants grown in acid sulfate soils (Tables 3 and 4), but since no symptoms of Cu deficiency were observed in the peat soil-grown plants, it was indicated that those plants must have developed a tolerance to low Cu concentration. The nutrient concentrations which were critical for sufficiency in the leaves of field crops were in the range of 24 to 70 in Fe (mg/kg), lower than 30 in Mn (mg/kg), lower than 3 in Cu (mg/kg), and ranged from 8 to 28 in Zn (mg/kg) [45]. Although the Cu and Fe concentrations in some plants were below critical levels, no symptom of Fe deficiency was observed. The levels of Mn and Zn in the peat soils of Thailand and Malaysia should be sufficient for plant growth. Mineral concentrations in plants grown in sandy podzolic soil. Mineral concentrations in sandy podzolic soil are very poor (Table 1), and the concentration of macronutrients is actually lower in sandy podzolic soil than in any other soil (Tables 3–6). The Al concentration in all of the plants studied
107 was relatively lower in this soil than in acid sulfate soils, especially for M. malabathricum (Tables 3 and 5). The Na concentration of some plants grown in this soil was high, regardless of the low exchangeable Na concentration in the soil (Tables 1 and 5). The Cu concentration was low in most plants, but not in all of them (Table 5). Mineral concentrations in plants grown in saline soils. The main vegetation in saline soils is mangrove, M. cajuputi and M. malabathricum, are not dominant, but these species can survive in these kinds of soils. A. ebracteatus and F. indica also survived in both acid sulfate soil and saline soil (Tables 3 and 6). Na concentrations in plant tissues were generally high except in the following species: Crotalaria macronala, Bridelia sp., Cissus sp., Stenochlaena paluustris, and M. malabathicum (Table 6). Nutrient balance in leaves M. malabathricum and M. cajuputi are widely adapted to various soils (Tables 2–7). Their notable characteristics are, for M. malabathricum, Al accumulation, and for M. cajuputi, Na accumulation, even in soils with respectively low Al and Na concentrations (Tables 3–7). Conversely, however, M. malabathricum and M. cajuputi respectively exclude or retain low concentrations of Na and Al, even in soils with high Na and Al concentrations. These species can also survive in Na-affected soils (Tables 3 and 6). Thus, some plants from these species were well adapted to both low pH soils (acid sulfate and peat) and saline soils. However, the mechanisms for both low pH (high Al) and high Na tolerance have not been elucidated until now, because it has been assumed that low pH tolerance and high Na tolerance are opposite phenomena, given the high pH of saline soils (Table 6). When M. malabathricum and M. cajuputi were grown in water culture, the growth of both species was stimulated by Al application (although M. cajuputi is an Al excluder plant) as was nutrient uptake, especially phosphorus uptake [13]. Because the pH around the rhizosphere decreased in M. malabathricum and M. cajuputi, such plants may solubilize Al-P precipitates [13]. Since the traits of Al and Na accumulation in leaves were found to be exclusive of each other and not coexistent, the nutrient balance was further examined, incorporating all data in this field survey (Tables 2–7). Data from the report of Geoghegan & Sprent [35] on the mineral concentrations of native plants grown in low pH soils in Central Brazil were also combined to help estimate the mineral correlations in leaves. Since the water culture experiments, including the various Al, Ca, Mg, and Si treatments of native plants in Thailand, were carried out in a greenhouse as described in previous reports [13, 17], data from these experiments were also combined to estimate the correlations. Ca and Mg are functional elements;
108
Figure 2. Correlation between elements in mature leaves of tropical plants.
however, as the Ca or Mg requirements in M. malabathricum are extremely low [17], it is assumed that the critical or functional level of Ca or Mg will vary among species, and this variation may in turn cause different responses to the levels of the other macroelements, N, P, and K. Garten [46] reported that high interelemental correlations exist among the elements N, P, K, Ca, and Mg in 54 species grown in the field. K in the alkaline metals and Ca and Mg in the alkaline earth metals correlate highly to each other, as well as to N and P [47]. Thus, functional elements accumulate mutually. N correlated positively with the macroelements P and K, but did not correlated with Ca and Mg (Figure 2). P and K also did not correlate with Ca and Mg. Since N, P, and K, among the macroelements, correlated with each other (Figure 2), the accumulation of these three elements is mutually interrelated. An antagonistic relationship between Al and all other nutrients, except for N and Mn, was discerned (Figures 2 and 3), indicating that low concentrations of other nutrients coinciding with high Al concentrations resulted from the plant’s own characteristics and not from environmental conditions. Note, for example, that large amounts of the other nutrients were supplied in the case of the water culture. Of the relationships between Na concentration and
109
Figure 3. Relationship between mineral concentrations and Al concentration. ∗ g/kg; N, P, K, Ca, Mg, and mg/kg; Fe, Mn, Zn, Cu, Na, Al. ; native plant grown in Thailand, ; native plant grown in Malaysia; ; native plant grown in the water culture cited from Osaki et al. [13] and Watanabe et al. [17], ; native plant grown in Central Brazil cited from Geoghegan & Sprent [35].
110
Figure 4. Relationship between mineral concentrations and Na concentration. ∗ g kg−1 ; N, P, K, Ca, Mg, and mg kg−1 ; Fe, Mn, Zn, Cu, Na, Al. Symbols are the same as Figure 3.
the concentrations of other nutrients, P-Na, K-Na, Zn-Na, Mn-Na, Cu-Na, and Al-Na were negative (Figures 2 and 4). Thus, Al and Na accumulator plants have a tendency to maintain a low concentration of other nutrients in their leaves, even if enough of the nutrients exist in the culture medium (for example in hydroponic culture). Fe also showed an exclusive relationship with other elements (Figures 2 and 5), although its negative relationship was not as strong as that of Al or Na. For these reasons, Al will form a complex with P in the root surface, at the cell surface, and in free space [48], preventing P translocation above ground. Al restricts the absorption of K in tea [49] and in maize [50]. Al can inhibit the absorption of Ca or Mg in upland rice [51], coffee [52], casaba [53], wheat [4, 5], Pinus radiata [54], maize [6], and many field crop species [55]. Al will compete with Mn in barley [8], sorghum [56], and maize [58]. Al also competes with Cu in potatoes [59] and sorghum [56].
111
Figure 5. Relationship between mineral concentrations and Fe concentration. ∗ g/kg; N, P, K, Ca, Mg, and mg/kg; Fe, Mn, Zn, Cu, Na, Al. Symbols are the same as Figure 3.
Thus, if Al exists in the culture medium, Al-sensitive plants will have their accumulation of nutrients reduced due to Al toxicity. However, since the growth of M. malabathricum (Al accumulator) and M. cajuputi (Al excluder) are stimulated by Al application [13, 17], the antagonistic relationship in these species between Al and other nutrients cannot be explained by the toxicity. It is well known that Na has an antagonistic effect on K, Ca, and Mg [11, 12], whereas the negative relationships between Na and other minerals such as Zn, Mn, P, Cu, and Al have not been generally recognized. Na concentration in the leaf was negatively correlated with K concentration (Figure 5), as was reported by Matoh et al. [12]; however, Na concentration was not correlated with the concentration of either Ca or Mg. High concentrations of P in soil appear to reduce Fe uptake due to an Fe-P complex [32]. The harmful effects of high Cu on Fe deficiency have been noted primarily under high Cu/Fe ratios [32]. Although high substrate Cu can reduce the Fe concentration in plants, the effect of Cu and the effects of other heavy metals in inducing Fe
112 deficiency appear to be complex. The ratio of Fe/(Cu+Mn), rather than that of Fe/Cu, has been a factor in developing Fe chlorosis in milo grown on two different soils. Fe and Mn are closely related in plant nutrition. For example, an excess of Mn causes a deficiency of Fe, and vice versa [32]. Hydroponic studies have shown by means of plant analyses that high levels of solution Mn can reduce the Fe concentration in the plant, while high levels of solution Fe can conversely reduce Mn concentration in the land. These results have been credited either to a mutual elemental antagonism or to oxidation-reduction reactions. Thus, to some extent, it is recognized that Fe has an antagonistic effect on other nutrients, including P, Cu, Mn, and Zn.
Acknowledgments We would like to express our gratitude to Dr Kunio Suzuki (Yokohama City University, Japan), Dr Prasarn Vongsaroj (Botany and Weed Science Division, Department of Agriculture, Bangkhen, Thailand), and Miss San-ang Homchen (Konken University, Thailand) for their helpful identification of plant species, assistance, and suggestion when the surveys were conducted. This research was supported in part by a grant from The Ministry of Education, Science, Culture, and Sports in Japan (07NP1201, 08NP0901, 09NP0901, 08406007, and 09460035), and by JSPS Tropical Bio-resources Research Fund.
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