Seedlings of Cedrela fissilis Vell. respond to single superphosphate application, but not to liming

ABSTRACT Cedro-rosa (Cedrela fissilis) is native to Brazil with great potential for seedling production. However, soil correction is necessary to improve its performance, due to the edaphoclimatic conditions in Brazil, where soils have a high weathering degree and large amounts of Fe and Al oxides. Here, we evaluated the combined effect of soil acidity correction by liming and phosphate fertilization using single superphosphate on the growth and development of cedro-rosa seedlings cultivated in Amazonian soil. The study was carried out in a greenhouse at the Universidade Federal Rural da Amazônia (UFRA) – Campus Capitão Poço, between July and December 2019. Different levels of base saturation (V%) showed no influence on the variables analyzed. On the other hand, phosphorus (P), calcium (Ca), and sulfur (S) supplied by single superphosphate significantly influenced growth and development of cedro-rosa seedlings. The optimum P levels for stem diameter (SD), leaves number (LN), root dry matter (RDM), stem dry matter (StDM), leaf dry matter (LDM), total dry matter (TDM) were 405, 286, 385, 421.87, 393.75, 445 mg dm-3 of P, respectively. Seedling quality (DQI) showed a positive linear response to levels of P, Ca, and S in single superphosphate. Thus, fertilization with P was necessary at the nursery stage for the cultivation of the species in soil of low chemical fertility. For better quality of cedro-rosa seedlings grown in pots, the application of 400 mg dm-3 of P is recommended.


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Sumbitted on August 11 th , 2022 and accepted on March 20 th , 2023.Seedling production is one of the most important stages for a productive and efficient forest stand; thus, providing the nutritional needs of seedlings optimizes seedling growth and initial establishment (Bognola & Maeda, 2012).
In this sense, knowledge of the soil chemical and physical characteristics is crucial at the nursery stage.
Moreover, in Brazil, production of forest seedlings is intense due to the expansion of agricultural areas and the high demand for wood products, leading to the exploitation of native remnants, intensive deforestation, and degradation of areas (Freitas et al., 2017).Therefore, revegetation of these areas is essential to improve the soil physical and chemical characteristics, providing the necessary protection through plant cover to reduce soil losses by erosion (Silva et al., 2011a).
Furthermore, the choice of the correct species to be cultivated is essential, given the soil and climate characteristics of the region.Research should focus on the use of native species at the nursery stage; nevertheless, few studies have investigated the production of native Tayssa Menezes Franco et al.
forest seedlings for timber production or recovery of degraded areas (Gonçalves et al., 2012).Most native forest species are poorly studied and scientific knowledge is needed to scale up seedling production with quality, such as cedro-rosa (Cedrela fissilis Vell.), facilitating crop management and reducing production costs (Oliveira et al., 2014).
Cedro-rosa is a forest species of the Meliaceae family and is classified as a late secondary successional species (Freiberger et al., 2013), widely distributed throughout the Brazilian territory (Pias et al., 2015).Cedro-rosa has good development in regions with deep, well-drained soils with a clayey to sandy-clay texture, as well as in temperate and humid climates at subtropical and tropical altitude (Angeli, 2005).
Cedro-rosa also has a high commercial value, with potential use in landscaping and in the production of high-quality wood (Martins & Lago, 2008).This species is also used in civil construction, frames, wainscoting, panels, linings, trimmings, packaging, musical instruments, and fine furniture (IPT, 2019).Thus, due to the environmental and economic importance of native tree species, mainly in seedling production, adequate nutrition is needed for the full development of cedro-rosa.
Most Brazilian soils are highly acidic under natural conditions with low nutrient availability, mainly phosphorus (P), due to high adsorption of phosphate ions to iron and aluminum oxides (Freitas et al., 2017).Therefore, practices to correct chemical constraints of the soil are necessary for the satisfactory development of cultivated species.Liming is an essential practice to correct soil acidity, as it neutralizes Al +3 and increases the pH, supplies Ca and Mg, improves the soil cation exchange capacity, increasing nutrient availability to plants (Ronquim, 2012) and favoring both root development and crop yield.
Brazilian forest species have shown a response to P application in nutrition and growth of Brazilian mahogany (Swietenia macrophylla King) seedlings (Silva et al., 2011b).The supply of 600 mg dm -3 of P 2 O 5 at 25% base saturation increased the growth of Cassia grandis Linnaeus seedlings (Freitas et al., 2017).To maximize the production of Australian cedar seedlings, the base saturation needs to be raised to 50% (Braga et al., 2015).
Organic and mineral fertilization in cedro-rosa showed that the combination of 10% of poultry litter with NPK fertilization provided better conditions for seedling development (Rego et al., 2021).However, few studies have investigated the effect of base saturation and P fertilization on the production of cedro-rosa seedlings.
Furthermore, it appears that native forest species have different responses to P fertilization and to soil acidity correction, which requires evaluations of these factors for the development of cedro-rosa seedlings.Thus, this study evaluated the combined effect of liming and P, Ca, and S fertilization by single superphosphate on the initial development of cedro-rosa seedlings grown in Amazonian soil.

MATERIAL AND METHODS
The experiment was carried out in a greenhouse at the Universidade Federal Rural da Amazônia (UFRA) -Campus Capitão Poço -Pará , between July and December 2019.In the region, air temperature ranges from 25.6 -26.9 °C with an annual average of air temperature of 26.2 °C (Pacheco & Bastos, 2001).The climate of the region is Am type (altitude tropical) (Köppen classification) with annual precipitation around 2,500 mm and a short dry season between September and November and relative humidity between 75 and 89% in the months with the lowest and highest precipitation volumes, respectively (Schwartz, 2007).The precipitation volumes and mean air temperatures were recorded during the experimental period (Figure 1).The main soil type of the region is the Oxisol (Soil Survey Staff, 2014), classified as Latossolo by the Brazilian soil classification system (Santos et al., 2018).
The soil used in the experiment was collected (0.20 -0.40 m) near the area of secondary vegetation on the premises of UFRA-CCP.Afterward, the soil samples were dried, sieved through a 2-mm mesh, and chemically analyzed (Table 1) at the laboratory of EMBRAPA -Amazônia Oriental (Belém -PA).
The results of the soil chemical analysis (Table 1) were used to calculate the need for liming, using the base saturation method (Raij, 1983) according to each treatment.The dolomitic limestone (Relative Power of Total Neutralization-"PRNT" = 98%) was mixed with the soil volume in each pot and placed to incubate for 30 days.
Cedro-rosa (Cedrela fissilis Vell.) seeds were obtained from the company Sementes Caiçara LTDA.The seeds were submitted to the dormancy breaking process by the imbibition method in distilled water for 24 h.Five seeds were sown in polyethylene bags (1 kg) filled with local soil.
The bags were placed in a screened nursery with 30% shading until the seedlings had four pairs of developed leaves.
Subsequently, thinning was performed and only the most vigorous plants were transplanted into plastic pots filled with 8 L of soil (Table 1).In these pots, the plants were grown in full sun (greenhouse without cover).
The experimental design was in randomized blocks with four replications in a 4 x 4 factorial scheme: four levels of base saturation-V (7.5, 20, 40, and 60%), equivalent respectively to 0, 1.65, 4.30, and 6.94 g of limestone pot -1 ), and four levels of P (0, 100, 200, and 400 mg dm -3 of P), using the single superphosphate source (18% P 2 O 5 , 16% Ca, and 8% S), which was applied to the soil surface in each pot (8 L).
During the experimental period, growth variables were measured monthly, such as plant height (PH), leaf number (LN), and stem diameter (SD).PH was measured with a graduated ruler, considering height from the ground level to the last apical bud.SD was obtained with a digital caliper and measurements were taken at 1 cm from the soil surface.For LN, a simple count of all fully expanded leaves of each plant was performed.
At 120 DAT, the plants were harvested and their parts were separated, dried in an oven with forced air circulation (70 ºC) until reaching constant mass, and weighed on an analytical balance to determination dry matter (DM).
as well as RDM/SDM ratio-and total dry matter -TDM (SDM+RDM) were determined.To collect the roots, the entire root system was washed under tap water in a sieve (2-mm mesh) to separate the soil.The Dickson quality index -DQI (Dickson et al., 1960) was estimated with the growth and DM variables (equation 1): where: TDM = total dry matter (SDM+RDM), in g; PH = plant height, in cm; SD = stem diameter, in mm; SDM = shoot dry matter, in g; RDM = root dry matter, in g.
Verification of normality assumptions (Kogomorov -Smirnov test) and homogeneity of variances (Bartlet and Levene tests) were carried out.Then, analysis of variance (ANOVA, p < 0.05) was performed to verify the effect of the factors and the interaction between the factors on the response variables.When significant, the results were adjusted to the regression models (linear and quadratic) and those with the highest determination coefficient (R 2 ) were chosen.The Tukey test was applied for base saturation (V) levels.In addition, Pearson's correlation coefficient (r) was estimated between the variables PH, SD, LN, RDM, StDM, LDM and DQI.All statistical analyses were performed using the Sisvar software (Ferreira, 2011) and the graphs were generated using Sigma Plot version 12.

RESULTS AND DISCUSSION
Analysis of variance showed a significant effect (p < 0.05) only for P levels (and Ca and S) by single superphosphate in all variables analyzed.The seedlings showed no response to base saturation levels through liming (Figures 1, 2, 3, and 4).However, it should be noted that each species responds differently to liming (Vieira et al., 2020).
In general, native tree species show satisfactory growth in acidic soils with low Ca availability (Furtini Neto et al., 2000), as observed in the conditions of the current study (Table 1).Furtini Neto et al. (1999) observed satisfactory growth of cedro-rosa seedlings in the treatment with only the Ca addition (12 mmol c dm -3 ) in the soil with an acidic pH, indicating that the species seedlings responded to the supply of Ca and not to the correction of acidity by liming.Fontes et al. (2013) found a similar result and reported that, in general, cedro-rosa did not show a significant response to liming in the production of total seedling biomass.The growth of Australian cedar, for example, was not affected by base saturation (60, 70, 75, and 80%) up to 150 days after planting the seedlings (Oliveira et al., 2015).In addition, liming did not show a significant effect on dry biomass production of Theobroma grandiflorum seedlings, when cultivated in a substrate with base saturation (BS) of 60% (Souza et al., 2021) and for the root biomass of Anadenanthera colubrina in BS of 24 and 60% (Gomes et al., 2004).
This pattern may indicate a protection mechanism for the species in which Al +3 bioaccumulates in the roots and is not translocated to the shoots; thus, keeping the photosynthetic apparatus functioning (Presotto et al., 2018) through the release of organic acids by the root system, which inhibits the effect of Al, giving plants the ability to raise the pH in the rhizosphere, reducing Al solubility and absorbing Al ions with subsequent immobilization in specific locations (Vale et al., 1996;Beutler et al., 2001;Hartwig et al., 2007;Presotto et al., 2018).
P fertilization and liming on Cassia grandis Linnaeus f. showed no significant responses for growth and biomass variables (Freitas et al., 2017).On the other hand, a significant effect of base saturation was observed in teak seedlings grown in a Red Oxisol (Favare et al., 2012).
Plant height (PH) responded linearly to single superphosphate fertilization (P, Ca, and S levels), while stem diameter (SD) showed a quadratic behavior to these nutrients supply, expressing the maximum value with the estimated level of 405 mg dm -3 of P (Figures 2A and 2B).The largest leaf number (LN) (7.19 leaves/plant) was obtained at the estimated level of 286 mg dm -3 of P, more than the double value without P application (Figure 2C).Increases in these biometric variables are essential for the survival rate of seedlings of forest species, especially due to adverse environmental conditions, such as dry spells and wind action.In addition, SD is essential for the financial return of the forester, due to wood production (Coneglian et al., 2016).
NPK doses in rainbow eucalyptus (Eucalyptus deglupta) showed a positive effect of P on the PH and SD of the seedlings (Pereira et al., 2021).The variables PH and SD showed a positive response to P addition in Açoita-cavalo (Luehea divaricata Mart.) seedlings for (Ceconi et al., 2006).P fertilization and mycorrhizal inoculation on mulungu (Erythrina velutina Willd.) and ipê-roxo [Handroanthus impetiginosus (Mart.ex DC) Mattos] seedlings showed a significant increase in PH, SD, and LN with increasing doses of P (Leite et al., 2014;Lopes, 2022).
Seedlings of Cedrela fissilis Vell.respond to single superphosphate application, but not to liming The response of plant growth (PH, SD, and LN) to P fertilization is consistent with low chemical fertility of the soil, mainly with low P availability (Table 1).In weathered tropical soils, the largest fraction of inorganic P is adsorbed by Fe and Al oxides, making P scarcity a limiting factor for plant growth in these environments (Novais et al., 2007).
P supply is essential for respiration and photosynthesis, as P is a component of ATP molecules.In addition, P partic-ipates in the formation of nucleic acids, coenzymes, and phospholipids.Thus, P is essential for the full development of plants (Bucher et al., 2018;Prado, 2020).P fertilization by single a superphosphate source provides Ca and S and theses nutrients may also improve plant growth.Ca is crucial for the middle lamella formation of the cell wall and S is a constituent of some amino acids and vitamins (Taiz et al., 2017;Kerbauy, 2019).For dry matter (DM) production of different plant organs, there was a response to single superphosphate supply, but not to liming (Figure 3).P fertilization promoted a quadratic response in RDM, StDM, and LDM and a positive linear response for SDM.For RDM, the maximum production (16.22 g plant -1 ) was obtained with the estimated level of 385 mg dm -3 of P (Figure 3A).
The adequate number of roots is essential for water and nutrient absorption by the plant, boosting plant growth (Kerbauy, 2019).Thus, biomass evaluation by the destructive method is also of great importance in the evaluation of seedling quality (Cruz et al., 2011).
The increase in biomass production observed on current study is related to the P, Ca, and S effect on plants by single superphosphate supply, which promote aerial and root growth and play a key role in metabolites related to Seedlings of Cedrela fissilis Vell.respond to single superphosphate application, but not to liming energy acquisition, and use and cell development (Prado et al., 2010;Taiz et al., 2017).Alves et al. (2015) observed an increase in shoot DM of Hymenaea stigonocarpa submitted to a single superphosphate rather than a triple superphosphate.
The estimated level of 421.87 mg dm -3 of P provided the maximum production (14.35 g plant -1 ) of StDM (Fig-

ure 3B
).On the other hand, the maximum LDM (12.40 g plant -1 ) was observed with the addition of 393.75 mg dm -3 of P (Figure 3C).Increasing P levels provided a linear increase in SDM production (Figure 3D).For the RDM/SDM ratio, a quadratic response was observed, decreasing with increasing P levels (Figure 3E).TDM showed a quadratic response to P levels (Figure 3F) in which the estimated level of 345.8 mg dm -3 of P provided the maximum TDM production (37.4 g plant -1 ) of cedro-rosa seedlings.Tayssa Menezes Franco et al.

Effects of P levels and liming have been assessed in
Red-Yellow Oxisol on seedling production of forest species (mahogany, cedro-rosa, sage, and Australian cedar) (Fontes et al., 2013).The authors reported a positive P effect on DM production, such as TDM.For cedro-rosa, the maximum TDM was obtained with the application of 200 to 300 mg dm -3 of P without a significant response to liming for this variable.P application had a positive linear effect on DM production of mahogany (Swietenia macrophylla King) seedlings cultivated in Yellow Oxisol (Santos et al., 2008).

P fertilization showed a quadratic effect on SDM of two
Eucalyptus genotypes with maximum production between 110 and 125 mg dm -3 of P (Novais & Ferreira, 2016).
The increase in soil base saturation (V%) did not influence the Dickson quality index (DQI) of cedro-rosa seedlings.On the other hand, a linear increase in DQI was observed with increasing P, Ca, and S levels by single superphosphate supply (Figure 4).Thus, P fertilization plays an important role for a higher survival rate of plants in the field, contributing to the success of forest stands and to the economic return of producers, as higher DQI confers higher seedling quality (Gomes & Paiva, 2012;Freitas et al., 2017).
There was a significant positive correlation (p < 0.05) between growth and biomass variables of cedro-rosa seedlings submitted to single superphosphate supply and limestone application (Table 2).
The high correlation observed between DQI and RDM was significant as well as the high correlation between DQI and SD and dry biomass variables, as they are important variables for seedling survival.Furthermore, LN is significantly correlated with DM production, as biomass is the final product of photosynthesis (Taiz et al., 2017).A positive correlation has been reported between the variables PH, SD, RDM, SDM, TDM, and DQI of Cassia grandis seedlings subjected to P levels and liming (Freitas et al., 2017).

CONCLUSIONS
Supply of P, Ca, and S is essential for the initial development of cedro-rosa seedlings grown in soil with low chemical fertility in the Brazilian Amazon.The application of 400 mg dm -3 of P in pots is recommended for better seedling quality.However, plants adapted to acidic soil do not need lime application in the initial growth phase.

Figure 1 :
Figure 1: Air temperature (Tair) and daily total precipitation (P) during the experimental period.

Figure 2 :
Figure 2: Plant height -PH (A), stem diameter -SD (B), and number of leaves -LN (C) of cedro-rosa seedlings as a function of P doses and base saturation levels (V%).Means followed by the same letters in the columns are considered statistically equal by the Tukey test (p > 0.05).

Figure 3 :
Figure 3: Dry matter production root-RDM (A), stem -StDM (B), leaf-LDM (C), shoot-SDM (D) RDM/SDM ratio (E), and tota l-TDM (F) of cedro-rosa seedlings as a function of P doses and base saturation levels (V%).Means followed by the same letters in the columns are considered statistically equal by the Tukey test (p > 0.05).

Figure 4 :
Figure 4: Dickson quality index (DQI) of cedro-rosa seedlings as a function of P doses and base saturation levels (V%).Means followed by the same letters in the columns are considered statistically equal by the Tukey test (p > 0.05).

Table 1 :
Soil chemical characterization (0.20 -0.40 m) used in the experiment pH -hydrogen ionic potential; P, K, and Na: extraction with Mehlich-1 and determination by colorimetry (P) and by flame photometry (K and Na); Ca, Mg and Al: extraction with 1 mol/L KCl and determination by atomic absorption spectrophotometer (Ca and Mg) and titration (Al); H+Al: extraction with Ca acetate pH 7.0 and determination by titration; CEC -cation exchange capacity.