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Phosphorus fractions in soil after successive crops of Pinus taeda l. without fertilization/Fracoes de fosforo apos cultivos sucessivos de Pinus taeda l. sem fertilizacao.


Soil management in Pinus forests should focus on the improvement of soil fertility in soils with low nutrient contents, as in the highlands in the South of the state of Santa Catarina. The Pinus forests of this region are often cultivated without fertilizer application, leading to a loss in the productive potential of the forests. Studies in South America and the South of the United States showed that fertilization at planting accelerated the growth of Pinus taeda (BEKELE et al., 2003; FAUSTINO et al., 2013; MORO et al., 2014), generating an economic return in response to this practice.

For the soil fertility diagnosis of annual crops, the available nutrient levels are measured by soil analysis, taking only the forms of easy desorption into account. In perennial and forestry crops, the diagnosis of phosphorus (P) availability is more complex, since the longer cycle, the greater is the possibility of buffering of the most labile by the less labile forms. Over the course of time, this increases nutrient availability in soils under Pinus stands, as emphasized by RICHTER et al. (2006); or in successive crops on unfertilized soil, as pointed out by GATIBONI et al. (2007).

In the forests, the P considered available by routine soil analyses (Mehlich 1 or anionexchange resin) ignores the less labile P forms that may become available, especially the labile organic forms (RICHTER et al., 2006). The common determination procedures do not detect the labile organic forms available to plants. Chemical fractionation of this nutrient allowed the identification from the most labile to the most recalcitrant forms. The subsequent use of chemical extractors with low to high extraction forces is the base to the technique of P chemical fractionation proposed by HEDLEY et al. (1982), which removed inorganic (Pi) and organic P (Po) from the more readily available to the most stable forms (GATIBONI et al., 2007).

The tool of chemical fractionation of P has become fundamental to the understanding of P dynamics in soils under Pinus stands, by indicating which fractions are accessible to plants. Improving the knowledge of the P dynamics between the different portions will make the establishment of new determination methods of P for Pinus crops possible, enhanced the precision of the technical recommendations of P fertilization. Thus, our hypothesis is that in successive forest crops without fertilization there is consumption of P forms other than available phosphorus, e.g., of the organic forms. In this study, we evaluated changes in the phosphorus fractions of an unfertilized Cambisol under successive Pinus taeda L. crops.


The study was carried out in Otacilio Costa, Santa Catarina (SC), in 16 and 17-year-old Pinus taeda L. forests, in the first and third crop, respectively, of which the latter reached 49 years of continuous Pinus cultivation. Two areas of the first and third crop took place, respectively, at the coordinates 27[degrees] 30' 03.38" S / 50[degrees] 05' 17.78" W and 27[degrees] 29' 59.92" S /50[degrees] 03' 25.84" W, at a distance of 1400m away from each other. The mean altitude of the region is 870m asl, and the climate is humid mesothermic (Cfb), according to the Koppen classification, with mild summers, a mean annual temperature of 15.9[degrees]C and annual rainfall between 1300 and 1400mm. In both areas, the soil was a Humic Cambisol according to the WRB/ FAO system, derived from siltstone of the Rio do Rastro formation; kaolinite is the predominant clay mineral and iron oxides and hydroxides are present in a lower proportion.

The studied stands were treated with the commonly used management for cellulose production, with a tree spacing of 2x3m and total absence of fertilization. Sampling areas were selected based on previous comparative soil surveys, to ensure homogeneity regarding soil type, altitude, sun exposure, and relief. In this way, were chosen two sites representing local forests, producing the first and third successive Pinus taeda crop, respectively. Due to the absence of an area with native vegetation near the experiments, with similar characteristics to those of the stand areas, it was decided to forgo the use of a control area without cultivation, avoiding a possible bias in the interpretation of results.

The equation: n = (t 2. C. V. 2)/E was used to calculated the number of sample points (n) per modal unit, where t: Student statistic at a probability level of 5%; CV: coefficient of variation (%) and E: sampling error (%), according to PELLICO NETTO & BRENA (1997). A sampling error of 15% was assumed, estimated based on preliminary samplings. Thus, soil samples collecting from six profiles (six sample points per modal unit of 750m2) from the layers 0-10; 10-20, 20-40, 40-60, and 6080cm. Samples were collected for chemical analyses and undisturbed samples in cylindrical rings to determine soil density. The experiment was arranged in a factorial design in strips (Factor A - cultivation period, with two levels, and Factor B - soil layers, with five levels).

The soil samples were oven-dried at 60[degrees]C, sieved through 2mm mesh, and the chemical and physical properties analyzed (Table 1), according to the methodologies described by EMBRAPA (2011), respectively. Forest litter was analyzed for carbon content (C) in samples collected in a 0.25m2 area, with three replications. In the field of the first crop, an amount of 16.5t [ha.sup.-1] of litter dry weight and a C content of 428g [kg.sup.-1] were reported while in the third crop these parameters were 21.6t [ha.sup.-1] and 403g [kg.sup.-1], respectively.

Phosphorus was chemically fractionated according to HEDLEY et al. (1982), modified according to CONDRON et al. (1985), as follows: samples of 0.5g dry soil were subjected to sequential extraction with anion-exchange resin (AER-Pi); NaHC[O.sub.3] 0.5mol [L.sup.-1] (NaHC[O.sub.3]-Pi and NaHC[O.sub.3]-Po); HCl 1.0mol [L.sup.-1] (HCl-Pi) and NaOH 0.5mol [L.sup.-1] + ultrasound (NaOH-Pi and NaOH-Po). After the extractions, the remaining soil was oven-dried and subjected to digestion with [H.sub.2]S[O.sub.4] + [H.sub.2][O.sub.2] + Mg[Cl.sub.2] (Residual-P). The Pi contained in the alkaline extracts NaHC[O.sub.3] and NaOH was determined by the spectrophotometric method proposed by DICK & TABATABAI (1977). In these alkaline extracts, total P was determined after digestion with ammonium persulfate + sulfuric acid in an autoclave (USEPA, 1971), and Po was computed as the difference between total P and Pi. The P of the acid extracts was determined by the spectrophotometric method of MURPHY & RILEY (1962).

The data were subjected to the Shapiro-Wilk normality test, and the non-parametric data were transformed into ranks to homogenize the variance, using the original data to interpret results. After that, the transformed data were subjected to analysis of variance. The means of data with significant effects (P<0.05) were compared by the paired Student's t-test (P<0.05) and the Scott-Knott test (P<0.05). For comparison of means of same layers between crops, the Student's t-test was used. The means between layers of the same crop were compared by the Scott-Knott test. The linear Spearman correlation was determined between the variables C, NaHC[O.sub.3]-Po and NaOH-Po and software SAS (SAS, 2007) used for statistical analysis.


Inorganic P fractions (Pi) extracted by anion-exchange resin (AER-Pi) and sodium bicarbonate (NaHC[O.sub.3]-Pi) did not differ between the Pinus crop rotations in any of the studied layers (Table 2). These fractions represented the forms considered labile and have a similar buffering capacity as P absorbed by the plants (GATIBONI et al., 2007). Studying modifications in the P fractions of a Cambisol, Oliveira et al. (2015) reported no differences between labile P fractions in a 10-year-old Pinus taeda stand in the first crop nor native forest, indicating that; although P-deficient, these soils have a good buffering capacity of these fractions. According to the criteria of Local Soil Fertility Committee, the AER-Pi levels indicated low (5.1 - 10) or very low P availability (<5.0), regardless of the crop, confirming that the soils are P-deficient, but have a good buffering capacity of the labile fractions.

The Po fraction quantified by sodium bicarbonate (NaHC[O.sub.3]-Po) differed between the crops, with higher values in the first crop down to the 40-60cm layer (Table 2). Values reported were approximately ten times greater than those of NaHC[O.sub.3]-Pi, indicating that the labile P forms in these soils are mainly stored in organic forms. In P-deficient soils, as those studied, the organic fractions play a fundamental role in the P cycle and plant nutrition (SLAZAK et al., 2010). These fractions were significantly correlated with soil C content (R: 0.73**), confirming that the presence of labile organic fractions is associated with organic matter accumulation.

The labile organic P forms probably buffer the inorganic forms, maintaining the labile inorganic P contents unchanged, even after three Pinus crops, as also observed by SLAZAK et al. (2010). Perennial plants have more time to take up P during the cycle than annual crops, so that slow-release forms, such as labile Po forms, can buffer the available P for the forest system. Consequently, for participating in the buffering of available P, the inorganic and organic fractions extracted from the soil by AER and NaHC[O.sub.3] should be quantified together to estimate the P availability for perennial plants.

Apart from the buffering of plantabsorbed P, another destiny of mineralized Po may be soil resorption on the surface of iron oxides (FINK et al., 2016). In the scheme of Hedley fractionation, the inorganic P fractions associated with higherenergy sites, e.g., silicate clays and oxides, are supposedly extracted by NaOH (GATIBONI et al., 2013). The Pi contents quantified by extractor 0.5mol [L.sup.-1] NaOH + sonication (NaOH-Pi) showed an increase of NaOH-Pi in the deepest soil layers under the third compared to the first Pinus crop (Table 2), indicating that this fraction acted as P drain. Most likely, P was redistributed in the profile due to the death of roots of previous crops and, in deeper layers, where there are less organic matter content and microbial activity, the soil adsorbs the mineralized phosphate.

Also, the low soil pH (Table 1) increases P adsorption capacity, favoring reactions with Fe and Al hydroxides, contributing to higher NaOH-Pi and Residual-P levels in the third crop. Conversely, in the soil surface layer the presence of organic matter reduces the P adsorption potential of the soil, competing with phosphates for the same adsorption sites on the surface of Fe and Al oxides and hydroxides (YAN et al., 2016).

Accumulation of organic matter near the soil surface aside from competing for the same adsorption sites as mineralized P and reducing the content adsorbed in NaOH-Pi increased the content of moderately labile organic P (NaOHPo). This fraction was higher in the soil of the third than the first crop in the 0-10cm surface layer (Table 2). This increase in NaOH-Po is expected in forest systems that promote C increase over time, where it comes to be a primary source in P-deficient soils (FINK et al., 2016). However, a reduction of C with time was observed, mainly in deeper layers, and also, the NaOH-Po fraction was not significantly correlated with C (R: [0.57.sup.ns]). Despite being considered higher energy forms, in situations of P deficiency, the P fractions bound to oxides and recalcitrant organic matter can participate in the buffering of the most labile fractions. Mainly for perennial plants, due to the longer extraction time of these crops (GATIBONI et al., 2007; OLIVEIRA et al., 2015).

The fraction HCl-Pi estimates the calciumbound P forms when still in primary minerals such as apatite or in rock phosphates applied to the soil (GATIBONI et al., 2013). In the soils of this study, the values (Table 2) were very low (<2 mg [kg.sup.-1]) in all layers of both forests, confirming that the soils of the southern region of Brazil are poor in P-containing primary minerals and were not treated with any rock phosphate fertilization.

Contents of remaining P in the soil sample, not extracted by any of the extractors of selective fractionation (Residual-P), indicating that it is highly recalcitrant, were lower in the 0-10cm and 10-20cm soil layers of the third than the first crop (Table 2). This fact indicated that continuous Pinus cultivation depleted the most recalcitrant P forms, pointing out that they can represent a P source in systems with a negative nutrient balance, (GUO & YOST 1998; GATIBONI et al., 2007).

About the relative distribution of P fractions in the soil, in all layers and periods of forest use, the recalcitrant (Residual-P) and moderately labile (NaOH-P) forms were the most abundant, since together they represented 87 to 97% of the total P extracted by fractionation (Figure 1). Nevertheless, percentages of labile P forms were small about the total P contents, with AER-Pi and NaHC[O.sub.3]-Pi together accounting for less than 1.1% in the first, and for less than 0.7% of the third forest crop. Conversely, NaHC[O.sub.3]-Po represented 8.5% in the first and 5.5% in the third crop, evidencing a reduction by Pinus cultivation. This fact showed that the labile P forms are mostly organic and that Pinus crops can access these fractions. However, even if these values are lower than those reported in other Pinus cultivation systems (BEKELE et al., 2003; RICHTER et al., 2006), there is no evidence of a response of Pinus to isolated P applications. In soils as that studied, the response to P applications is except just at the beginning of the stand (MORO et al., 2014).

Ratio between the labile and moderately labile inorganic forms ([AER-Pi + NaHC[O.sub.3]-Pi]/ NaOH-Pi) may indicate the balance between these P forms and the dynamics involving them, which theoretically are the most management-sensitive (Figure 2A). In the soil of the third crop, the proportion of labile inorganic was lower than of the moderately labile forms. Similarly, the labile organic decreased about the moderately labile forms (NaHC[O.sub.3]-Po/NaOH-Pi) from the first to the third crop, indicating an increase in less labile Po over time of forest use, or even the consumption of part of labile Po (Figure 2B). The same behavior was observed in the relationships between labile and moderately labile, organic and inorganic forms ([AER-Pi + NaHC[O.sub.3]-Pi + NaHC[O.sub.3]-Po]/ [NaOH-Pi + NaOH-Pi]) (Figure 2C).

This reduction can be explained by the different equilibrium times of the P fractions, where the removal of P in solution by plant uptake destabilizes the balance between the fractions. This fact causes a domino effect, which, over time, causes all P fractions to contribute to the maintenance of the contents in solution (GUO & YOST, 1998; GATIBONI et al., 2007). Nevertheless, it should be emphasized that while buffering by the most labile forms is fast, it is slower by the more recalcitrant forms, due to the higher binding energy of P to colloids. Therefore, the desorption rate of the most recalcitrant forms may fail to supply the plant demand, as pointed out by GATIBONI et al. (2007). However, the critical level of P varies mostly between crops and that the relevance of the buffering of the labile by the most recalcitrant forms will therefore also be variable.

Assuming the existence of a temporal continuity in the soil between the first and third crops the P would be a decreasing trend in the contents of the first (more labile) fractions of the fractionation with the forest use, indicating a consumption of inorganic and organic labile forms. Concomitantly, the most recalcitrant (Residual-P) forms would decrease, since a part of the released phosphorus would be readsorbed in moderately labile Pi and Po forms (NaOH-P). In this way, all the soil P forms would be in equilibrium, and the forest use would cause a slow P stepwise desorption effect, where the decrease in P availability in the most labile fractions would trigger a replenishment process, involving all forms of soil P, including the most recalcitrant. Experiments that investigated the exhaustion of available soil P using successive crops without phosphate fertilization, such as those of GUO & YOST (1998) and GATIBONI et al. (2007), pointed out the contribution of all soil P forms, including the most recalcitrant, to plant supply.

Results of this study reinforced the need for greater research efforts towards the establishment of new prediction criteria of P availability in perennial crops such as Pinus taeda, given the ability of these crops to exploit P fractions that are indefinable by traditional methods. Although, low P rates applied to Pinus proved promising in the soils of this region (MORO et al., 2014), the plant growth capacity in these P-poor soils in one of the areas of the world with highest Pinus productivity is surprising (CARDOSO et al., 2013). This fact reinforced the idea that the critical levels established for annual crops were not applied to perennial crops, such as Pinus taeda, and that new criteria are required, which are likely to be much lower. In this sense, in the new update of the Manual of Fertilization of

Soils of Southern Brazil, published by the Local Soil Fertility Committee (CQFS-RS/SC, 2016), different critical P levels are recommended. The new critical level depends on the soil type and crop requirements, and the forest species are newly classified as "low response" plants. Studies of calibration and response to phosphate fertilization of Pinus should be promoted, including analyses of the availability of P methods capable of quantifying the labile organic and inorganic fractions, e.g., the method based on 0.5mol [L.sup.-1] NaHC[O.sub.3].


Successive Pinus taeda L. cultivation without soil fertilization decreases the phosphorus contents in labile inorganic and organic forms and the buffering of these by less labile forms. In soils cultivated with Pinus taeda L., labile organic P should be considered an auxiliary parameter to be used together with labile inorganic P to diagnose the phosphorus availability and fertilization requirement.

Received 06.21.16 Approved 04.04.17 Returned by the author 05.11.17


The authors would like to thanks the Klabin Inc. for the financial support, Project FIEPE/CAV - KLABIN n[degrees] 07, 29/08/2008.


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Luciano Colpo Gatiboni (1) * Cristiane Ottes Vargas (1) Jackson Adriano Albuquerque (1) Jaime Antonio Almeida (1) James Stahl (2) Djalma Miller Chaves (2) Gustavo Brunetto (3) Daniel Joao Dall'Orsoletta (1) Luiz Paulo Rauber (4)

(1) Universidade do Estado de Santa Catarina (UDESC), Av. Luis de Camoes 2090, 88520-000, Lages, SC, Brasil. E-mail: * Corresponding author.

(2) Departamento de Pesquisa e Desenvolvimento Klabin S.A.

(3) Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brasil.

(4) Universidade do Oeste de Santa Catarina (UNOESC), Santa Catarina, SC, Brasil.

Caption: Figure 1 - Percentage distribution of the soil phosphorus fractions extracted by Hedley's chemical fractionation from a Humic Cambisolols under successive cultivation of Pinus taeda in the 1st crop after 16 years (a) and in the 3rd crop with 17 years (b), both without fertilizer application for 16 and 49 years, respectively.

Caption: Figure 2 - Relation between the fractions of AER-Pi and NaHC[O.sub.3]- Po (a) fractions of NaHC[O.sub.3]-Po and NaOH-Po (b) and fractions of labile P (AER-Pi, NaHC[O.sub.3]-Pi and Po) and moderately labile Pi and Po (NaOH-extracted) (c) from soil under Pinus taeda forests, in the 1st and 3rd crop. Bars represent the standard error of the mean; Means followed by capital letters between the crops in the same layer do not differ from each other by the t test (P<0.05); Means followed by equal lowercase letters between layers within the same crop do not differ from each other by the Scott-Knott test (P<0.05).
Table 1--Chemical and physical characterization of soil in six
layers, under Pinus taeda cultivation, in the first and third crop.

Layer   pH water         C          Al    Ca    Mg     K      P

cm                 g [kg.sup.-1]     [cmol.sub.c]      mg [kg.sup.-1]

                               Pinus in the 1st crop

0-10      4.3           36         9.6    7.0   2.5   65.0   8.2
10-20     4.4           30         8.2    8.4   2.5   67.0   6.0
20-40     4.5           31         10.4   7.2   2.1   61.0   2.2
40-60     4.4           31         6.1    4.0   2.0   55.3   1.2
60-80     4.4           23         6.6    3.0   1.5   59.4   1.8

                                Pinus in the 3rd crop

0-10      4.0           33         12.3   0.5   1.2   36.3   5.7
10-20     4.1           31         10.3   0.7   1.1   25.0   2.5
20-40     4.1           29         9.7    0.4   1.4   28.4   1.1
40-60     4.2           15         8.7    0.6   1.0   31.6   1.8
60-80     4.3            8         9.1    0.5   1.0   32.5   2.6

Layer   Sand   Silt   Clay    m      V

cm         g [kg.sup.-1]          %

            Pinus in the 1st crop

0-10    182    336    482    49.8   15.1
10-20   147    415    438    42.5   17.0
20-40   120    278    602    52.4   13.7
40-60   120    278    602    49.8   10.6
60-80   145    259    596    58.7   8.1

          Pinus in the 3rd crop

0-10    178    358    464    87.2   2.9
10-20   228    359    413    84.4   3.0
20-40   236    255    509    83.6   3.0
40-60   197    354    449    83.6   3.2
60-80   180    264    556    85.0   3.0

m: aluminum saturation; V: base saturation.

Table 2--Phosphorus contents in the different forms of Hedley
fractionation and sum of the P contents extracted from the soil
of Pinus taeda forests in the first and third crop.

Layer      AER     NaHC[O.sub.3]   NaHC[O.sub.3]    NaOH       NaOH

            Pi          Pi              Po           Pi         Po

cm                           mg [dm.sup.-3]

                          Pinus in the 1st crop

0-10      8.8 aA      3.4 aA          70.6 aA      19.0 aA   288.2 aB
10-20     6.4 aA      1.9 bA          67.6 aA      16.5 aA   323.5 aA
20-40     3.6 bA      0.9 bA          46.6 bA      13.3 bB   285.2 aA
40-60     2.2 bA      1.5 bA          28.4 cA      14.0 bB   138.2 aA
60-80     1.8 bA      2.7 aA          15.8 cB      9.2 bB    186.7 aA
CV% (1)    43.4        35.2            40.8         28.6       57.0

                                                Pinus in the 3rd crop

0-10      5.3 aA      2.3 aA          39.8 aB      22.4 bA   404.0 aA
10-20     2.4 bA      1.8 bA          30.4 aB      18.2 bA   322.4 bA
20-40     1.1 cA      1.7 bA          15.9 bB      24.9 bA   281.2 bA
40-60     1.9 cA      0.5 dA          16.2 bB      34.8 aA   215.1 cA
60-80     3.0 bA      1.2 cA          26.1 bA      31.5 aA   157.5 cA
CV%        30.6        25.2            37.1         19.9       28.9

Layer      HCl     Residual P   [SIGMA]


cm              mg [dm.sup.-3]

             Pinus in the 1st crop

0-10      1.1 bA    440.7 bA    830.7 aA
10-20     1.1 bA    432.9 bA    849.8 aA
20-40     0.7 cA    401.7 bA    752.8 aA
40-60     1.3 bA    606.5 aA    791.1 aA
60-80     1.8 aA    543.4 aA    759.9 aA
CV% (1)    29.7       32.2        39.8

             Pinus in the 3rd crop

0-10      0.5 aA    242.6 bB    718.0 aA
10-20     0.6 aA    278.7 bB    654.6 aB
20-40     0.2 bA    301.2 bA    625.4 aA
40-60     0.2 bA     463 aA     732.7 aA
60-80     0.7 aA    493.4 aA    714.9 aA
CV%        44.6       21.2        36.1

(1) CV% Coefficient of variation of the data; Means followed by
capital letters between the crops in the same layer do not
differ from each other by the t test (P<0.05); Means followed
by equal lowercase letters between layers within the same crop
do not differ from each other by the Scott-Knott test (P<0.05).
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Author:Gatiboni, Luciano Colpo; Vargas, Cristiane Ottes; Albuquerque, Jackson Adriano; Almeida, Jaime Anton
Publication:Ciencia Rural
Article Type:Ensayo
Date:Jul 1, 2017
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