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Boron in humus and inorganic components of Hamra and Grumosol soils irrigated with reclaimed wastewater.


Boron (B) is involved in important soil processes (Kovda 1973): the intra-soil biological cycle; humification; isomorphic substitution in clay minerals and the formation of colloids; and illuviation. Goldschmidt (1937) found that B is concentrated in the uppermost humus layer of forest soils. Viets (1962) supposed that much of the B in soils is complexed with humus, probably as adsorbed, chelated, or complexed ions, where its release to plants is presumably dependent on soil moisture. Berger and Pratt (1963) stated that a large part of the total B in soils is held in the organic matter in tightly bound compounds that have been formed in the growing plants themselves; B in organic matter is primarily released as available form through the action of microbes. Agulhon (1910) showed that B stimulates the growth of several vascular plants in water culture and that B is abundant in lignified tissues. Matoh et al. (1992) assigned 95-98% of the total plant B to cell wall under B-limiting conditions, leaving only a small fraction for possible involvement in other plant functions. Increasing evidence suggests one or more functions of B beyond cell-wall structure for a large variety of organisms, including plants, animals, and bacteria. Several critical reviews of B chemistry and its role in higher plants have been published since 1997 (Hu and Brown 1997; Nable et al. 1997; Power and Woods 1997; Dembitsky et al. 2002; Bolanos et al. 2004; Goldbach and Wimmer 2007; Tanaka and Fujiwara 2008; Kot 2009; Lehto et al. 2010).

Knowledge on biogeochemistry of B in soil-plant systems may be crucial for most cultivated soils of different climatic areas, including those deficient in water resources and forced to utilise down-graded and reclaimed wastewater (RWW). Wastewaters tend to be relatively high in B concentration, mostly due to its presence in detergents. Studies on B fertilisation have shown that the limits between B deficiency and toxicity are very narrow, and that applications of B can be extremely toxic to some plants at concentrations only slightly above optimum for others (Cartwright et al. 1984; Gupta et al. 1985). Irrigation water does not usually contain enough B to injure plants directly; rather, it is the continued use and concentration in the soil due to evapotranspiration that leads to the eventual toxicity problems (Eaton and Wilcox 1939; Gupta et al. 1985). In general, both total and plant-available B can be very high in arid or semi-arid areas where leaching is limited.

Boron is a constituent of cell walls and membranes of vascular plants and is also essential for algae, diatoms, and cyanobacteria, whereby it enters soil humification processes. Though studies on B in soil and soil-plant systems focus mostly on inorganic B interactions, a few works have considered B-organic/humus forms in soil (e.g. Kot 2009). Unlike most other micronutrients, plant roots require a continuous external supply of trace amounts of B, otherwise loss of membrane function occurs within minutes (Blaser-Grill et al. 1989; Asad et al. 1997). Like other micronutrients, the minimum solution concentrations of B required for plant growth are too low to be easily measured directly. These concentrations must be low enough not to have an adverse effect on plants. For example, rapeseed (Brassica napus) requires ~ 10 [micro]g B/L in the transpiration stream (Asad et al. 1997). Until recently, no reliable measurements of B content in soil solution <10 [micro]g/L were available with which to confirm the above estimates in the field (Bell 1997). Moreover, the published data were obtained by means of procedures that included filtration through 0.45-[micro]m membrane filters (although other sizes between 0.2 and 1.0 [micro]m have also been used); the earlier works utilised paper or cellophane filters of rather irregular pore size. In fact, such samples of soil water do not represent a real soluble phase, but a heterogeneous water-mobile phase that may include organic biopolymers (e.g. fulvates and humates, polysaccharides, and exocellular biopolymeric material, low-weight organic complexes), clay minerals, mineral precipitates (e.g. iron (Fe), aluminium (Al), manganese (Mn), or silicon (Si) hydro-oxides, carbonates, phosphates), and biocolloids including viruses, bacteria, and protozoans (Buffte et al. 1992; Kretzschmar and Schafer 2005). Boron determined in such samples could not serve as evidence of the presence of dissolved inorganic boric acid or borates in the soil liquid phase. Obviously, the content of available B compounds in the real soil water mobile phase must be controlled by an effective buffer system that could supply trace but continuous quantities of B.

Reviewing the literature on soil B chemistry, one finds information on soil B association with various soil components, including adsorbed/exchange forms and those occluded in mineral phases (e.g. clays and Fe/A1 hydro-oxides), as well as the common assertion that dissolved B compounds occur as undissociated boric acid and borates in soil solution, which are generally supposed to be major bioavailable forms of B. Only a few works have considered the necessity of including B-organic forms in their fractionation schemes (Viets 1962; Hou et al. 1994, 1996; Yermiyahu et al. 2001; Raza et al. 2002; Lemarchand et al. 2005; Kot 2009). The published data on B in humus fractions should be treated with caution, as the commonly utilised procedures are able to extract only a part of soil humus. As yet, investigators of soil humus have not elaborated a generally accepted approach and terminology (see Kononova 1966; Greenland 1971; Schnitzer and Khan 1972; Ponomareva and Plotnikova 1980; Orlov 1985; Stevenson 1994). The International Humic Substances Society (IHSS) has made an attempt to introduce a standard extraction procedure tbr humus (humic) material based on the procedure of Swift (1996). However, this procedure allows only humates and fulvates bridged to solid soil particles through divalent (calcium, [Ca.sup.2+]; magnesium, [Mg.sup.2+]) cations to be extracted; it affects neither (1) humates complexed firmly to clays and sesquioxides (through polyvalent [Fe.sup.3+]/[Al.sup.3+]/titanium ([Ti.sup.4+]) cations) nor (2) the refractory fraction of humin (Tyurin 1937; Brcmncr et al. 1946; Kawaguchi and Kyuma 1959; Russell and Russell 1961; Kononova 1966; Greenland 1971; Duchaufour 1977; Ponomareva and Plotnikova 1980; Orlov 1985; Stevenson 1994), including the extractable fraction of humin (Preston et al. 1994). As Stevenson (1994, p. 44) stressed: 'The organic matter not extracted with alkali (humin) is believed to exist at high-molecular-weight polymers or at humates associated with sesquioxides and silicates. Complete extraction of soil organic matter has yet to be achieved, even after numerous alternative base and acid treatments.'

In some classic works on soil humus (Waksman 1936; Tyurin 1937; Russell and Russell 1961 ; Kononova 1966; Aleksandrova 1980; Ponomareva and Plotnikova 1980; Orlov 1985), the authors distinguished, among others, a fraction of humic and fulvic acids bridged to solid soil particles through calcium, and a fraction of humic and fulvic acids bound firmly to clay minerals and refractory sesquioxides. The latter fraction is especially enriched in heavy clay soils (Ponomareva and Plotnikova 1980). Szucs and Elek (1962) found that B concentration tends to decrease with depth, reflecting changes in the humus-clay complex. Duchaufour (1977) distinguished three main types of organo-mineral complexes in soils of temperate areas: humus-CaC[O.sub.3] in calcareous soils, humus-allophane in andosols, and humus-Fe in brown acid soils. The fractions of humu-Fe/Al complexes and humin were rarely included in soil humus fractionation schemes, even though they may account for a substantial portion of soil organic matter.

The objectives of this work were to evaluate: (1) the major fractions of soil B with special emphasis on humus and water-mobile phases; and (2) changes in the soil B forms and mobility due to utilisation of RWW. The presented work is based on the detailed humus fractionation procedure described in Ponomarcva and Plotnikova (1980) grounded on the approach of Waksman (1936) and Tyurin (1937).

Materials and methods


Two Mediterranean soils were examined: Hamra (red sandy loam; FAO: Luvisols, Chromic Luvisols; USDA: Rhodoxeralf, Haploxeralf); and Grumosol (dark clay carbonaceous; FAO: Vertisols; USDA: Chromoxerert, Pelloxerert). Detailed description of both soils may be found elsewhere (Singer 2007).

The Hamra soil samples were taken from a lysimeter experiment in which the soils were irrigated with fresh water and RWW for 5 and 7 years, and are hereafter referred to as Hamra Fr 5, Fr 7, Rcl 5, and Rcl 7, respectively. Sampling was done at three depths: 0-5, 5-25, and 25-45 cm. The samples were taken from three lysimeters (repetitions) and blended in equal proportions. The Grumosol was sampled in a field experiment at the Acre Station, western Galilee. The two soil plots, 15 m apart, had been irrigated for 4 years, one with fresh water, the other with RWW (secondary treatment) and are hereafter referred to as Grumosol Fr 4 and Rcl 4. The RWW were supplied from the Shomrat reclamation plant reservoir. Samples were collected within the profile at four depths: (0-2, 2-5, 5-15, and 15-25 cm. The estimated inputs of B in the soils treated with RWW were: 7 [+ or -] 3 and 9 [+ or -] 3mg B/kg soil for Hamra Rcl 5 and Rcl 7, respectively, and 7 [+ or -] 3 mg B/kg soil for the Grumosol Rcl 4.

Some major chemical and physico-chemical parameters for the soils are given in Figs 1 and 2 and for the RWW in Table 1.


Air-dried and sieved (1-mm) samples were processed by a series of chemical extractions with subsequent determination of B utilising the ICP-AES technique. The extraction scheme (Table 2) was developed based on a common fractionation (Tessier et al. 1979) extended for the detailed fractionation of soil humus (Waksman 1936; Tyurin 1937; Greenland 1971; Aleksandrova 1980; Ponomareva and Plotnikova 1980; Preston et al. 1994). In this work, the term 'humus' refers to the extractable and non-extractable soil organic humified matter, which includes humic and fulvic acids (humates and fulvates) and humin.


The conditional character of nominal fractions has been widely discussed in the literature. As many researchers emphasise, it is not possible to achieve extraction with no sample loss, contamination, or change. A combination of separation techniques and element-selective detection systems is typically required for this kind of analysis. Unfortunately, such techniques alter the native species in a sample, as the chemical equilibrium is affected and contaminations and losses are often seen. In this case, no analytical procedure, no matter how sophisticated, will successfully reflect the native situation (Salomons and F6rstner 1984; Martin et al. 1987; Tack and Verloo 1995; Michalke 1999). Nevertheless, although no extraction scheme can provide true species-specific information, such protocols can provide data regarding the biogeochemically relevant fractionation of trace elements in soils and sediments (Salomons and Forstner 1984; Martin et al. 1987).


The following humus fractions were obtained: (1) humic and fulvic acids bridged to solid soil particles through divalent (Ca/Mg) cations (Ca/Mg-humates and fulvates) (step 4, Table 2); (2) humic and fulvic acids complexed firmly to aluminosilicates with polyvalent cations (Fe/Al humate and fulvate complexes) (step 5); (3) extractable part of humin (steps 8 and 9); and (4) refractory non-extractable humin/ organic matter, according to content of organic carbon ([] in residue after step 9. To obtain extractable humin, a 1-month dissolution procedure with diluted (5 vol.%) hydrofluoric (HF) and hydrochloric (HCI) acids was utilised (Preston et al. 1994) in place of concentrated HF, and it does not affect the organic matter significantly during the dissolution of aluminosilicates (step 8).

Boron in fractions of easy-reducible (amorphous Fe/Mn) minerals and Fe/Al amorphous and crystalline minerals (free, non-silicate Fe) was determined according to Tamm (1922), Mehra and Jackson (1960), and Schwertmann (1964) (steps 6 and 7).

Boron in the exchangeable phase was determined according to two procedures: (1) Han and Banin (1995) elaborated specifically for carbonaceous soils, and (2) the more commonly adopted extraction with Mg[Cl.sub.2] solution (Tessier et al. 1979).

Mannitol-extractable B was determined to evaluate the potentially bioavailable portion of the element (Hingston 1964; Cartwright et al. 1984; Nable et al. 1997). We did not utilise the method of hot water B extraction, as many researchers marked significant problems associated with this method, such as precision and high variability in the results, and problematic comparability of the basic soil parameters determined routinely (e.g. Sah and Brown 1997; Miller and Vaughan 1999; Shiftier et al. 2005). The amount of B extracted by this method is affected by the extraction time and temperature (Spouncer et al. 1992) and the potential re-adsorption of B during the cooling period (McGeehan et al. 1989). On the whole, the hot-water extraction procedure is difficult to standardise (Novozamsky et al. 1990), time consuming, and tedious for routine usage if reproducible results are to be obtained (de Abreu et al. 1994).

Soil-water extracts (1 : 1 and 1 : 5 ratios) were obtained after centrifugation at 2000rpm and filtration through membrane filters of 1.20, 0.45, and 0.20 [micro]m to separate mobile water components. Content of B and other parameters (pH and electrical conductivity (EC)) were also determined in each filtered fraction. Absorbance at 465 and 665nm was measured to evaluate content and type of soluble/mobile organic matter in the water extract (factors E4 and E6) (Chen et al. 1977; Chin et al. 1994).

Some basic soil parameters were also determined by the commonly adopted methods: pH and EC of soil-water suspension (1:2) (Peech 1965; Bower and Wilcox 1965); content of [] by Walkley-Black method as described in Allison (1965); Fe and Al in humus extracts and residual fraction; content of sodium (Na), potassium (K), Ca, and Mg in exchangeable fraction, Ca and Mg in carbonates and humus fractions, Fe and Mn in fractions of easy-reducible minerals, Fe and Al in fraction of free (non-silicate) amorphous and crystalline minerals, and A1 in fraction of aluminosilicates. All devices (high-grade polypropylene and high-density polyethylene) in contact with the samples and extracts were pre-cleaned by filling with or soaking in 3% nitric acid (HN[O.sub.3]) solution for 48 h. The detection limit for B, calculated as three times the standard deviation of the blank, was 0.01 mg/kg.

Results and discussion

Application of the RWW resulted in noticeable changes of several key characteristics of the soils, namely exchangeable cations, EC, content of B, [], and more (Figs 1 and 2). In the Hamra soil, content of [] (Fig. 1) increased by up 1.5 times in the Rcl 7 treatment compared with the Fr 5, mostly in the uppermost 0-2 cm horizon, in contrast, in the 0-2 cm layer of the Grumosol, the [] content somewhat decreased in the Rcl treatment. The RWW was an additional source of organic matter and at the same time a contributor of high microbial activity, potentially inducing a priming effect (Sorensen 1974), particularly in the Grumosol. Organic matter is also a major reducing agent in soil, which may have affected B binding to amorphous Fe and Mn minerals. The slightly alkaline RWW (pH 7.6 [+ or -] 0.4) increased the mean pH values in the slightly acidic Hamra soils by 0.7-0.9 units in the upper 0-5 cm and by 1.4-2.3 units in the deeper 5-25 cm layer, whereas pH balance was not affected significantly in the clayey calcareous Grumosol. Acidity/alkalinity of soil (pH conditions) is often considered as one of the most important factors affecting availability of soil B. However, as Shorrocks (1997) stressed, except in the case of the adverse effects of liming on B availability, soil pH per se appears to have little practical bearing, via its effect on adsorption by clay minerals and aluminium and iron oxides. The EC of the water extract varied greatly, with the maximum in the surface layers of the soils irrigated with the RWW indicating the accumulation of soluble salts. Content of exchangeable cations was increased due to the application of RWW in the Hamra soil, although irrigation with RWW did not affect it significantly in the Grumosol most probably due to much higher exchange and buffer capacity (Fig. 2).

Irrigation with the RWW did not greatly affect the total B content in the Grumosol (Fig. 1), which ranged from 32.5 to 34.7 mg/kg in the Fr plot and from 38.2 to 43.1 mg/kg in the Rcl plot, and yet the difference showed accumulation of B in the Rcl plot. This accumulation in the top layers is roughly consistent with the added B amounts via the RWW during 4 years of irrigation. In the Hamra soil, the maximum B content was found in the Rcl 5 plot (irrigated with RWW for 5 years) at 38.8-45.8 mg/kg, and the minimum in the Rcl 7 plot (irrigated with RWW for 2 years longer) at 21.7-28.6 mg/kg, probably a result of the more intensive leaching in the light Hamra soil, particularly after 7 years of irrigation, followed by the rain events during winter. Plant uptake of B under RWW might also contribute to the increased B removal from the soils (results not shown).

Boron in water-mobile and potentially bioavailable compounds

In soils, water-soluble and exchangeable phases, carbonates, easy-reducible (Fe/Mn) amorphous minerals, and labile organic compounds are the substances most vulnerable to chemical and microbial attack; B bound to these compounds is hence potentially available for biota.

In the Hamra soil, the concentration of B in the soil : water 1:1 and 1:5 extracts filtered through a 0.45-[micro]m filter was rather high, comprising ~7% (3-11%) of the total element content. Surprisingly, B was not detected in <0.20-[micro]m water filtrates, indicating preferential binding of B to coarse mobile colloids (presumably, bacterial cells and cellular debris, colloids of clay, carbonates, and phosphates; Buffle et al. 1992). Additionally, B was not detected in the 1 M Mg[Cl.sub.2] extract from the suspended/colloidal matter detained by the 0.20-[micro]m and 0.45-[micro]m filters (data not shown), indicating that B was bound firmly (non-exchangeable) to the colloid particles. Thus, the soil water extract contained <10 [micro]g B/L (the detection limit of the ICP used in this study), which is a very low concentration (Gupta et al. 1985; Barber 1984; Aitken et al. 1987). In the water extract from the Fr 5 plot, B was found in the filtrate of >0.20-<0.45 [micro]m only, while the application of RWW resulted in an increased B concentration in the coarser phase >0.45 [micro]m (Fig. 3), presumably due to the enhanced growth of microorganisms in the soils irrigated with RWW.

In the heavier clayey Grumosol, water-mobile B compounds were detected in the filtrate >0.45 [micro]m only (Fig. 3), constituting, on average, 0.2% of total B in the surface Fr and 0.7% of total B in the surface Rcl soils, and were decreased to 0.0% and 0.4% in the deeper layers, respectively. The concentration of water-mobile B compounds in the Grumosol was an order of magnitude lower than that of the Hamra soil. The probable explanation is higher binding and adsorbing capacity of the Grumosol due to higher content of Fe/Al minerals and fine clay material. For example, the content of total Fe was 640-1060 mg Fe/kg in the Hamra soil, compared with 2310-2800 mg Fe/kg in the Grumosol; the content of clay was 10.0% in the Hamra soil and 61.5% in the Grumosol.


In the Hamra soil, for the water filtrate <0.45 [micro]m, the absorption at wavelengths of 465 and 665 nm (factors E4 and E6) gave a meaningful correlation with the content of B for the Rcl plots (r= +0.66, P < 0.05), but not for the Fr plots. This may indicate different origin and forms of B in the water-mobile B fraction of the Fr and Rcl plots. For both Fr and Rcl plots, the spectrophotometric data indicated the presence of fulvic(-like) substances, according to the E4/E6 ratio of 8-11 (Chen et al. 1977; Ponomareva and Plotnikova 1980).

Thus, although the water-mobile B compounds constituted a significant portion in the Hamra soil and a detectable portion in the Grumosol, the dominant part of these forms was watermobile coarse colloids >0.20 [micro]m, while B compounds related to finer colloids <0.20 [micro]m and the presumable dissolved species were below detection. However, B content in the filtrate >0.20 [micro]m showed a significant positive correlation with B content in the mannitol extract (r=+0.79, P<0.05; Table 3).

Boron was not detected in the exchangeable phase of both Hamra and Grumosol soils, extracted with either 1 M N[H.sub.4]N[O.sub.3] or 1 M Mg[Cl.sub.2]. The treatment with 1 M Mg[Cl.sub.2] solution could extract both exchangeable cations and anions. Su and Suarez (1995) reported that B[(OH).sup.0.sub.3] and B[(OH).sup.[?].sub.4] species adsorbed firmly on Fe and Al minerals via a ligand exchange. Some studies also addressed B sorption on natural organic matter (Yermiyahu et al. 2001; Lemarchand et al. 2005; Keren and Communar 2009). Hingston (1964) and Yermiyahu et al. (2001) reported higher sorption of B on soil organic matter than on clay; at similar pH levels and total B concentration, the sorption was 1-2 orders of magnitude higher than on clays. Sorption/desorption studies of B (as boric acid) on organic matter exhibited strong hysteresis effects and the sorbed B was removed to a partial extent only (Keren and Communar 2009). The formation of dihydroxy- and/or hydroxy-/carboxy-binding of borate to humic substances and/or carbohydrates was proposed to be the main sorption mechanism (Yermiyahu et al. 2001). Our results showed an absence (or very low content) of B species on the exchange sites of the investigated soils.



The absence of detectable concentrations of soluble and exchangeable B compounds raises the question of the source and mechanism of plant-available B supply in these soils. It is generally assumed that undissociated boric acid and, at higher pH, borates are those B forms that are directly consumed by plants and microbiota from soil solution and exchange sites. However, to the best of our knowledge, no direct evidence has been published on the presence of B in 'solutions' of regular soils as free dissolved boric acid or borates. Lindsay (1972) expressed this premise in a cautious way: 'Only two soluble B species in soils can be expected'. Moreover, until recently there were not adequate analytical facilities to determine B concentrations at trace ([micro]g/g) level (Downing et al. 1998), and especially to distinguish B chemical species in soil solution directly. Moreover, most experiments--either in hydroponics or in the field--on B behaviour in soil and biota have been based on supplying inorganic solutions of boric acid and borates. As Viets (1962) stressed, soluble borate added to soil is weakly adsorbed and remains largely in the water-soluble phase where it can be toxic to sensitive species. In fact, the experiments with inorganic solutions of boric acid and borates showed that plants are able to take up B (as oxy-B complexes) from the applied inorganic solution, but these experiments do not prove that the same processes take place in situ soil plant system. As Hu and Brown (1997) pointed out, the apparent contradiction between experimental results and in-field observations suggests that B uptake is determined by factors that are as yet unknown. More recent studies have provided new evidence that could probably explain these apparent contradictions. Dordas and Brown (2000) supposed that differences in B uptake are due to the differences in lipid composition of the plasma membrane of plant cells. It remains unclear whether differences in B uptake between cultivars can be wholly ascribed to differences in lipid composition (Tanaka and Fujiwara 2008).

Several investigations allow the supposition of a major role of organic/humus matter in soil B mobility and availability. Some authors considered the possibility of direct uptake of fulvic acids and low molecular weight organic complexes by plant roots (Schallinger 1984; Cheng and Coleman 1990) and bacteria (Steinberg and Munster 1985) with B bound to them (Lehto et al. 2010). At least one bacterial species (Arthobacter) was reported to utilise fulvic acids directly (De Haan 1977). Many authors supposed that most of the soil micronutrients are complexed by organic chelators which act as a buffer for nutrient supply (Treeby et al. 1989). The formation constant for the metal-chelate complex, the excess of chelator in solution, and the solution composition govern the activity of the micronutrient elements in solution. These systems are able to maintain sub-micromolar concentrations of micronutrients. For the case of B (B-oxy complexes), such a chelator must be of a specific nature. Asad et al. (1997) evaluated a range of possible B chelators and borosilicate glass for their effectiveness in maintaining solution B concentrations for water culture studies, including groups of polyhydric alcohols, sugars, phenolic compounds, and fluoride. They found that the B-specific resin containing N-methyl-glucamine functional groups (Kunin and Preuss 1964) appeared to be very promising as a solution buffer to regulate B concentration in solution.

The content of B in the carbonate fraction (Fig. 4) increased slightly due to irrigation with RWW, in the Grumosol from 0.18 (0.14-0.19) mg/kg in the Fr plot to 0.27 (0.21-0.33) mg/kg in the Rcl plot, and in the Hamra from 0.37 (0.25-0.60) mg/kg in the Fr plots to 0.68 (0.39-1.02) mg/kg in the Rcl plots, respectively. Similar levels of B have been found for the fraction of easy-reducible (Fe/Mn) amorphous minerals (Fig. 4).

Mannitol-extracted B has been demonstrated to be closely correlated with B taken up by plants (Hingston 1964; Cartwright et al. 1984; Nable et al. 1997). In the Hamra soils, the concentration of B in the mannitol extract was 0.18 (0.11-0.25) mg/kg in the Fr plots and 0.38 (0.32-0.49) mg/kg in the Rcl plots; in the Grumosol, this value was 0.33 (0.30-0.35) mg/kg in the Fr plot and 0.39 (0.32-0.42) mg/kg in the Rcl plot (Fig. 4), which is approximately the same concentration level as in the fractions of carbonates, easy-reducible Fe/Mn minerals, and Ca/Mg-fulvates. Correlation analysis (Table 3) showed that the mannitol-extracted B in both soils correlated well with content of B in carbonates, and in the Grumosol also with B content in HaO-mobile colloids (>0.20[micro]m), easy-reducible (Fe/Mn) amorphous minerals, and Ca/Mg-fulvates. This implies that the B supply to vegetation and microbiota may depend on the above soil fractions and that the bioavailable B may be dependent on pH (indicated by B in the carbonates) in both soils, and on redox conditions (B in the Fe/Mn minerals) and mobile humus compounds (B in the Ca/Mg-fulvates) in the Grumosol. Irrigation with RWW increased the mannitol-extracted B content in the Hamra soil, by 2.1 on average, despite the significant increase of pH in the Rcl plots. In the Hamra soil, the mannitol-extracted B showed a close statistical correlation (r=+0.72, P<0.05) with B content in the carbonates, a pH-vulnerable soil component. In the Grumosol, both parameters changed insignificantly.


Boron in major humus and inorganic fractions

In the Hamra soil, most B was found in extractable humus compounds (Fig. 5a), on average 54% (28 71%) of the total B content, along with the fraction of free (non-silicate) Fe/Al amorphous and crystalline minerals (step 7). Among humus fractions, most B was associated with Fe/Al-humate complexes (step 5, Table 2) and the extractable part of humin (step 9) (Fig. 6), i.e. soil organic compounds that are resistant to chemical and bacterial attack. Only a small quantity of B was determined in the residual fraction (refractory residue, Fig. 5a), left after all of the sequential extraction procedures--on average 1.3% (0.7-2.4%) of the total B content. This fraction presumably reflects B binding to the soil components most resistant to chemical treatment, i.e. insoluble organic matter/humin (including non-humified plant residue as lignin, waxy cuticles, paraffin) and minerals of the tourmaline group.

In the carbonaceous and clay-rich Grumosol, extractable B-humus compounds were the third-largest B fraction--an average of 9% (5-13%) of the total B (Fig. 5b), comprising mostly extractable humin-B and Ca-humate-B in the Fr plot and extractable humin-B and Ca-/Fe-humate-B complexes in the Rcl plot (Fig. 6). Most of the B (along with a significant part of [], Al, and Fe) was determined in the refractory residue--on average 52% (40 63%). Possibly, the mix of diluted hydrofluoric and hydrochloric acids used to extract this fraction (step 8, Table 2) has not been effective enough for the clayey Grumosol. We can suppose that, in the Grumosol, a significant part of B may be bound to non-extractable organic matter and refractory inorganic compounds.

In the soils investigated, B in the Ca/Mg-humate/fulvate fractions, i.e. the humus fractions obtained according to the IHSS procedure (step 4, Table 2; Fig. 6), only contained ~5-18% of the total B in the Hamra soil and 3-6% in the Grumosol. As mentioned above, the IHSS procedure makes it possible to extract only that part of soil humus bridged to soil particles via divalent cations ([Ca.sup.2+], [Mg.sup.2+]). It is also known that humates and fulvates serve as binding agents for the cohesion of clay particles through H-bonding and coordination with polyvalent cations such as [Ca.sup.2+], [Mg.sup.2+], [Fe.sup.3+,] [Al.sup.3+,] and [Ti.sup.4+]. The divalent cations do not form strong coordination complexes with organic molecules and would only be effective to the extent that a bridge linkage could be formed. Organic matter bound in this manner should be rather easily displaced by a monovalent cation, such as during the regular extraction procedure with a 0.1 M (or 0.2-0.5 M) sodium hydroxide solution. In contrast, [Fe.sup.3+] and [Al.sup.3+] form strong coordination complexes with humic substances, in which case displacement of the bound metal is difficult (Greenland 1971; Cameron et al. 1972; Ponomareva and Plotnikova 1980; Stevenson 1994) and may require extraction with a strong chelating agent (Stevenson 1994), by multiple alternative treatments with solutions of acids and alkalis (Tyurin 1937), or by applying heat in alkaline solution (Cameron et al. 1972; Ponomareva and Plotnikova 1980). The major portion of humus B in the studied soils was bound firmly to refractory humus fractions, including humin and humus-Fe/Al complexes, which cannot be affected by the procedure recommended by the IHSS. The more complete extraction of the soil humus showed that B is much more organophilic than is often supposed.

According to the specific B content, on a weight basis, the extractable humin and Fe/Al-humate/-fulvate complexes were found to be the most effective B carriers. For the Hamra soil, the range was as follows (on average, mg B/g []): humin-extractable (10.8)>humic acid (HA)-Fe (4.0)>fulvic acid (FA)-Fe (3.0)> HA-Ca (0.6)> FA-Ca (0.4).

The B preferentially binding to humus compounds supports the hypothesis of soil humus origin from lignin (Waksman 1936); most of the soil humus-B originates in the plant litter. We can assume that the bulk of B in the soil-plant system circulates among plants (lignin of cell walls and membranes) and the soil organic matter/humified material (see Berger and Pratt 1963); the soil organic matter/humified material, in turn, may serve as a source of B to the plants. For example, Lehto et al. (2010) stressed that for forest ecosystems, the major fluxes in the B cycle are within the ecosystems. The processes in the rhizosphere--microbial activity, root excretion and uptake, and release of B from organic sources to soil water, all affecting B mobility and availability--are still poorly understood. The role of organic/humus matter may be of major importance in these transformation processes.


In the soils studied, the major part of B was found in humus fractions, mostly in refractory fractions of humin, Fe/Al-humates, Ca/Mg-humates, and organic/inorganic nonextractable residue; this supports Waksman's (1936) theory of soil humus origin from plant lignin. It can be assumed that the bulk of B in the soil plant system circulates among plants (lignin) and the inherited soil organic/humus matter. The procedure of soil humus extraction recommended by the IHSS is not sufficient to evaluate B fractionation in soil as it recovers only a part of humus-bound B. In water extract, B was detected in the coarse colloid fraction >0.20 [micro]m, presumably of organic origin (bacterial cells and/or fulvic complexes). No exchangeable B was detected in the soils as well. The absence (or rather low content) of soluble and exchangeable B raises the question of the source (and mechanism) of B supply to vegetation/biota. It is noteworthy that irrigation with RWW resulted in a significant increase, by 2.1 times, of mannitol-extractable B in the Hamra soil but not the Grumosol, and redistribution of the humus B fractions in favour of Fe/Al-humate complexes in both soils.


We thank Dr Lira A. Matyushkina, Institute of Water and Ecological Problems, Far Eastern Branch of the Russian Academy of Sciences, Khabarovsk, Russia, for the constructive remarks on the manuscript. We would like to express our sincere gratitude to the anonymous reviewers whose remarks and notes brought about improvements to the manuscript. Financial support provided by Misrad ha-Klita, State of Israel, is appreciated.

Received 7 September 2011, accepted 16 January 2012, published online 20 February 2012


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F. S. Kot (A,B), R. Farran (A), M. Kochva (A), and A. Shaviv (A)

(A) Faculty of Civil and Environmental Engineering, Technion-Israel Institute of Technology, Haifa 32000, Israel.

(B) Corresponding author. Email:
Table 1. Parameters of the reclaimed wastewater from the Shomrat
reclamation plant reservoir (Oved et al. 2001; Bernstein et al. 2009)
BOD, Biochemical oxygen demand

EC pH N[H.sub.4.sup.+]-N
(dS/m) (mg/L)

1.4 [+ or -] 0.1 7.6 [+ or -] 0.4 18.8 [+ or -] -8.6

Total N BOD Boron

28.8 [+ or -] 12.0 44.6 [+ or -] 22.4 0.55-0.7

Table 2. Extraction scheme for soil boron fractionation

Step Procedure Fraction/extract

 extraction procedure

1 1.1 [H.sub.2]O, filtered Water/mobile
 subsequently through components/colloids
 1.20-, 0.45-, and
 membrane filters

 1.2 1 M Mg[Cl.sub.2], Exchangeable B on
 from 0.20-[micro]m coarse colloid
 filter suspended material

2 I M NaAc I-HAc Carbonates
3 3.1 1 M Exchange cations

 3.2 1 M Mg[C1.sub.2] Exchange cations and

4 0.1 M NaOH separated The IHSS method
 at pH 2 into:

 4.1 Acid-insoluble Humate-Ca/Mg

 4.2 Acid-soluble Fulvate-Ca/Mg
5 0.02 M NaOH, water complexes
 bath, 6 h, separated
 at pH 2 into:

 5.1 Acid-insoluble Humate-Fe/Al

 5.2 Acid-soluble Fulvate-Fe/AI

6 0.1 M hydroxylamine Easy/reducible (Fe/
 hydrochloride Mn) minerals

7 Na-dithionite- Free (non/silicate)
 citrate buffer

 Fe/Al amorphous and
 crystalline minerals

8 HF+NCI, 5 vol.% Clay minerals
 each, l month,
 occasional stirring

9 0.02 M NaOH at Humin extractable

10 HN[O.sub.3]+HCI at Refractory residue
 60[degrees]C for 72h Separate suhsample

11 0.05 M mannitol+0.01 (Potentially)
 M Ca[C1.sub.2] pH 8.5 bioavailable B

Step References

1 1.1


2 Han and Banin (1995)
3 3.1 Han and Banin (1995)


4 Swift (1996)


5 Ponomareva and
 Plotnikova -1980



6 Tamm (1922);

7 Mehra and Jackson

 Schwertmann (1964)

8 Preston et al.

9 Preston et al.


11 Cartwright et al.

Table 3. Correlation matrix for mannitol-boron and potentially
bioavailable boron fractions in the Hamra and Grumosol soils
irrigated with fresh and reclaimed wastewater

Only significant correlation coefficients are presented (* P<0.05,
*** P<0.001)

 [H.sub.2]0-mobile B in B in easy-
 B (>0.20 pm) carbonates reducible
Mannitol-B +0.79 * +0.72 * 10.74 *
[H.sub.2]O-mobile B -- 10.83 * 10.99 ***
 Hamra soils
Mannitol-B -- +0.72 * 0.76 *
[H.sub.2]O-mobile B --

 B in

Mannitol-B +0.78 *
[H.sub.2]O-mobile B +0.93 ***

[H.sub.2]O-mobile B
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Date:Feb 1, 2012
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