The Fate of Soil-Applied Nitrogen in the Fig Tree

Abstract

The timing of nitrogen fertilizer application in an orchard can determine the amount of nitrogen (N) absorbed, distributed, and accumulated in fig tree organs. This study aimed to evaluate the fate of nitrogen (N) applied to the fig tree at different times in the soil. The experiment was conducted in the 2009–2010 crop season. The planted trees belonged to the cultivar Roxo de Valinhos, in the São João Del Rei municipality of Minas Gerais state (MG), Brazil. The treatments were the application of 20 kg N ha⁻¹ as urea, enriched with 2% excess ¹⁵N atoms, on September 30 (T1) or on October 30 (T2). In January 2010, the fig trees were cut down and separated into fruit, leaves, new shoots and shoots from previous years, and the stem. The harvested parts were dried, weighed, and ground. Soil was collected from the 0.00–0.10 and 0.10–0.20 m layers, dried, and ground. The total N and excess ¹⁵N atoms in the organs and in the soil were determined, and the N derived from the fertilizer was calculated. The annual organs of the fig tree, including leaves, fruit, and young shoots, exhibited the highest accumulation of N from soil application at both timings, with similar N uptake and accumulation levels. However, nitrogen fertilization had a minimal contribution to the overall nitrogen content in young trees and did not exceed 11%. Understanding the fate of nitrogen derived from fertilizer within the fig tree’s organs will allow for more precise adjustments when recommending nitrogen doses.

1. Introduction

Minas Gerais (MG) state has the third largest area planted to fig trees (Ficus carica) in Brazil. The crop holds great social and economic importance because it is one of the main sources of income for rural producers, mostly family laborers. The cultivation occupies around 2097 hectares [1]. In the microregion of Campos das Vertentes, as well as in the municipality of São João Del Rei, fig tree orchards are in general established on medium-depth soils, loam or clay texture, and acidic with low or medium organic matter contents, which supposedly provide low mineral nitrogen (N) supply capacity for the plants [2,3]. However, sometimes, the soil between plant rows has intense growth of cover plant species that cohabitate with the fig trees and may take up nutrients, including N, from deeper soil layers. If cover crop plants are leguminous, they may additionally promote biological fixing of atmospheric N. During the decomposition of plant remains from cover crops or fig trees, including senescing roots, nitrogen (N) contained within the plant tissue can be released into the root zone of fig trees. While this contributes to the nutrient requirements of fig trees, to some extent, fertilization remains necessary [4,5]. The fig tree has no peculiarities in terms of its root system since it does not need rootstocks. Under favorable conditions, root distribution is concentrated closer to the trunk and may account for up to 50% of the total volume. However, in less favorable conditions, roots can extend to considerable depths [6].

The fig tree, like other fruit-bearing species, takes up soil N, especially in mineral forms such as nitrate (NO₃⁻-N) and ammonium (NH₄⁺-N), which is then incorporated into the tree biomass and temporarily accumulated in the growing organs, such as leaves, fruit, and new shoots [7,8,9]. At the end of the cycle, N may be redistributed and accumulated in the form of N compounds in perennial organs, especially the roots, and in the following cycle, N may be mobilized and redistributed to the annual organs [8,10]. Thus, the quantity of N taken up by fruit-bearing species, like the fig tree, should both meet the current season demands and the need for the formation of N reserves. However, the N of the fertilizer applied is not always utilized and accumulates in large quantities in the annual and perennial parts of the plant [11,12]. This may occur because of the period of application of N rates, which in the Minas Gerais state, has been established in September, coinciding with the bud break phase; in October, which is the period of rapid growth of the new shoots; and in December, which is near the maturation and harvest of the fruit [13]. However, N fertilizer must be supplied in periods of greater demand, which are not completely known yet. Soil availability of nitrogen, both from fertilization and soil mineralization, undergoes great variations, which might be assessed only by regional field experiments.

There is limited knowledge regarding the optimal timing for N application in fig trees. The timing of application can affect the amount of N absorbed by the fig tree from the fertilizer. Identifying appropriate times for N supply stands as one of the most effective strategies for enhancing N absorption from fertilizers, thereby reducing the potential for N losses, particularly nitrate (NO₃⁻) [3,10]. The timing of N fertilizer application can influence the nitrogen accumulation in both the annual and perennial organs of fig trees. However, the distribution of N fertilizer within these organs is not sufficiently understood, particularly in fig trees. The nitrogen isotope (¹⁵N) works as an efficient marker for determining the optimal timing and targeted organs for nitrogen (N) fertilizer application and has already been used in grapevines [8,14], peach [10], pears [15], apples [16], and citrus [17]. This technique facilitates the tracking and quantification of labeled N accumulated in the plant’s organs, enabling insights into the fate of applied N in the plant [5]. The present study aimed to evaluate the fate of soil-applied N affected by the timing of supply using ¹⁵N-enriched fertilizer as a tracer for nitrogen in fig trees.

2. Materials and Methods

The study was conducted in a commercial fig tree (Ficus Carica L.) orchard of the Roxo de Valinhos cultivar in São João Del Rei (MG), Brazil (latitude: 21°06′17.57″ S; longitude: 44°15′02.87″ W; altitude: 917.44 m), in the 2009 and 2010 crop seasons. The fig tree orchard was established in 2007, with a density of 2666 plants per hectare (1.5 × 2.5 m) and open center training. The soil was classified as an Oxisol [18] and, in the 0–20 cm layer before implementation of the experiment, it exhibited the attributes shown in

Table 1. Physical and chemical characteristics of the soil at the experimental site at 0.0–0.20 m depth.

Soil Characteristics	Value
Clay (pipette method) (g kg−1) [19]	37
Organic matter (Walkey–Black method) (g kg−1) [20]	1.80
pH in H2O (1:1 ratio) [20]	5.5
Exchangeable Al (extractor KCl 1 mol L−1) (cmolc kg−1) [20]	0.00
Exchangeable Mg (extractor KCl 1 mol L−1) (cmolc kg−1) [20]	0.10
Exchangeable Ca (extractor KCL 1 mol L−1) (cmolc kg−1) [20]	0.30
Availability P (extractor Mehlich-1) (cmolc kg−1) [20]	29.3
Availability K (extractor Mehlich-1) (cmolc kg−1) [20]	22

. The climatic data obtained during the period of the experiment is presented in

Table 2. Average rainfall and air temperature data during the experimental period.

Year-Month	Rainfall (mm)	Air Temperature (°C)
2009
September	98.4	20.8
October	246.6	20.7
November	149.6	22.6
December	310.3	21.5
2010
January	273.6	22.9

.

In 2007, three months before planting the fig tree, dolomitic limestone was applied on the soil surface, with later incorporation in the 0–20 cm layer to raise the base saturation up to 70% [13]. The base saturation determination method was determined by [19]. The treatments consisted of the application of 20 kg N ha⁻¹ in the form of urea enriched with 2% excess ¹⁵N atoms on September 30 (T1) or on October 30 (T2) 2009. At the time of N application, native herbaceous vegetation present on the orchard soil was eliminated in an area of 0.50 × 0.50 m (0.25 m²) around the stem of the fig tree. The urea was applied to the soil surface. The soil was irrigated manually immediately after the N application, using a watering can with the addition of 1.5 L of water per plant, to reduce N losses through volatilization. Throughout the experiment, the 0.25 m² area was kept free of weeds. Spontaneous plants like Bidens pilosa L. and Brachiaria decumbens Stapf were maintained between rows and, when necessary, they were subjected to mowing.

A randomized block experimental design was used with three replications; each plot was formed of five plants, but measurements were taken from the three central plants. The plants had a comparable number of productive branches, and blocks were distributed along the orchard. Throughout the experiment, the fig trees received the application of potassium chloride (58% K₂O) and triple super phosphate (46% P₂O₅), with doses of 50 kg and 60 kg, respectively. The fertilizers were applied in August, during the dormant period.

On 5 January 2010, the fig trees were cut down and separated into fruit, leaves, new shoots, shoots from the previous year, and stems. All the organs were dried in a forced air oven type MA035/2 (Marconi Equipamentos para Laboratórios, Piracicaba, SP, Brazil) at 65 °C until constant weight and, soon afterwards, ground in the Willey-type knife mill MA340 (Marconi Equipamentos para Laboratórios, Piracicaba, SP, Brazil) and stored for analysis. In the 0.25 m² area around each fig tree where N was applied, a trench was opened, and soil samples were collected from the 0.0–0.10 and 0.10–0.20 m layers. These samples were then dried and ground, along with the tissue samples, and sent to the Soil Analysis Laboratory at the Federal University of Santa Maria (UFSM). In the laboratory, samples were prepared in triplicate for all analyses. Total N and excess ¹⁵N atoms in the fig tree organs and in the soil were determined by a continuous flow isotope ratio mass spectrometer, Hydra 20/20 (Sercon, Crewe, UK). With the results obtained, the atoms of excess ¹⁵N (Equation (1)) and fertilizer N (Ndff) (Equations (2) and (3)) in the fig tree organs and in the soil [8,10] were calculated according to the procedure described by [21].

The atom% ¹⁵N excess was calculated according to Equation (1):

Atom% ¹⁵N excess in sample (%) = atom% ¹⁵N in sample − 0.3663% (natural abundance of atmospheric ¹⁵N isotope)

(1)

The N derived from fertilizer (%Ndff) was calculated using Equation (2):

Ndff (%) = (atom% ¹⁵N excess in sample/atom% ¹⁵N excess in fertilizer) × 100

(2)

The N derived from fertilizer (Ndff) (mg) was calculated using Equation (3):

Ndff(mg) = (Total N in sample (mg) × (atom% ¹⁵N excess in sample)/(atom% ¹⁵N excess in fertilizer)

(3)

The results obtained were subjected to an analysis of variance and a Tukey means comparison test at p < 0.05 to assess differences between the application timings. The statistical program Sisvar vesion 5.6 (Federal University of Lavras, Statistics Departament, Lavras, MG, Brazil) was used to conduct the analyses [22].

3. Results

In the fig trees subjected to the application of 20 kg N ha⁻¹ in September 2009, the highest dry matter yield was observed for the stem (131.93 g plant⁻¹), which did not differ statistically from the values observed for the leaves (95.37 g plant⁻¹) and shoots (81.53 g plant⁻¹) from the previous year (

Table 3. Dry matter, total N, excess ¹⁵N atoms, and N derived from fertilizer (Ndff) in fig tree organs subjected to different times of N application.

Organ	Dry Matter (g plant−1)	Total N		Atom% 15N (Excess in Sample)	Ndff
		(%)	(mg plant−1)		(% of Total N in the Organ)	(mg plant−1)
September
Leaves	95.37 ab (1)	2.49 a	2298.4 a	0.1529 a	7.64 a	175.71 a
Fruit	18.07 c	1.39 b	251.2 b	0.1084 ab	5.42 ab	13.61 b
New shoots	36.47 b	0.87 c	317.3 c	0.1400 a	7.00 a	22.21 b
Shoots from the previous year	81.53 ab	0.51 d	415.8 c	0.0533 b	2.66 b	11.08 b
Stem	131.93 a	1.46 b	1926.2 b	0.0440 b	2.20 b	42.38 b
Total	363.4 A	-	5208.9 A	-	-	264.99 A
October
Leaves	82.87 c	1.14 bc	943.2 b	0.1993 a	9.96 a	93.99 b
Fruit	35.53 c	1.52 b	541.7 b	0.2028 a	10.14 a	54.93 b
New shoots	205.60 b	2.85 a	5864.1 a	0.1370 ab	6.85 ab	401.69 a
Shoots from the previous year	362.50 a	0.49 d	1790.9 b	0.0552 b	2.76 b	49.43 b
Stem	208.50 b	0.74 cd	1545.1 b	0.0547 b	2.73 b	42.26 b
Total	895.0 A	-	10,685 A	-	-	642.47 A

⁽¹⁾ Mean values followed by the same lowercase letter in the column do not differ among the plant organs within the same period of N application and the capital letter in the same column, but between the time periods of N application, do not differ among themselves by the Tukey test (α = 0.05).

).

The greatest total N content was found in the fig tree leaves (2.49% and 2298.4 mg plant⁻¹). The greatest percentages of excess ¹⁵N atoms were observed in the leaves (0.1529), fruit (0.1084), and shoots from the previous year (0.1400). The greatest percentages of N derived from fertilizer were seen in the leaves (7.64), new shoots (7.00), and fruit (5.42). But also, the percentage obtained in the fruit did not differ statistically from that observed in the shoots from the previous year and stem. On the other hand, the greatest quantity of N derived from fertilizer was recovered in the leaves (175.71 mg plant⁻¹).

In the fig trees subjected to the addition of 20 kg N ha⁻¹ in October 2009, the greatest dry matter yield was obtained in the shoots from the previous year (362.50 g plant⁻¹) (Table 3).

The greatest percentage and quantities of total N were observed in the new shoots, 2.85% and 5864.1 mg plant⁻¹, respectively, which differed from the other organs. The greatest percentages of excess ¹⁵N atoms were seen in the fruit, leaves, and new shoots, matching the results of excess ¹⁵N atoms in the organs of the fig trees subjected to the application of N in September 2009. The greatest percentages of N derived from fertilizer were observed in the fruit (10.14), leaves (9.96) and new shoots (6.85). The fruits exhibited percentages of N derived from fertilizer equal to those observed in the leaves from the new shoots. In addition, the new shoots exhibited the greatest quantities of N derived from fertilizer (401.69 mg plant⁻¹).

The Ndff was accumulated preferentially in annual active organs as the leaves (September) or the news shoots (October), at all times of N application (Figure 1) rather than in perennial parts, such as the shoots from the previous years and stems or yet the fruits (annual organ).

The timing of N supply has not affected the soil N content or the excess ¹⁵N atoms in the 0.00–0.10 and 0.10–0.20 m layers (

Table 4. Total N concentration, ¹⁵N excess, and N derived from fertilizer (Ndff) at depths of the soil planted to fig trees and subjected to different times of N application.

Soil Layer Depth (m)	Application (time)	Total N (%)	15N Excess (Atom % 15N)	Ndff (% of Supplied N)
0.00–0.10	September	0.13 ± 0.01 a	0.0457 ± 0.0086 a	2.28 ± 0.42 a
	October	0.16 ± 0.02 a	0.0406 ± 0.0100 a	2.03 ± 0.50 a
0.10–0.20	September	0.10 ± 0.01 a	0.0135 ± 0.0036 a	0.67 ± 0.17 a
	October	0.09 ± 0.01 a	0.0377 ± 0.0235 a	1.88 ± 1.17 a

Mean values followed by the same letter in the column do not differ among themselves by the Tukey test (α = 0.05).

). Total N, excess ¹⁵N atoms, and N derived from fertilizer tended to be greater in the 0.00–0.10 m layer, likely because the nitrogen fertilizer was applied on the soil surface without incorporation, which is in agreement with other studies that used ¹⁵N as a tracer.

4. Discussion

The highest percentages and quantities of nitrogen (N), whether total or derived from fertilizer, were observed in the annual organs such as leaves, fruits, and new shoots of fig trees. This is attributed to the rapid cell division in these organs, which act as nitrogen sinks during the fig tree’s vegetative and productive cycle, thereby increasing dry matter production and nutrient demand, including nitrogen (references). Similar phenomena are well documented in other fruit-bearing species, such as grapevines [5,8], peaches [10], and apple trees [23]. However, perennial organs, such as shoots from previous years and stems in fruit-bearing species, serve as transitional nutrient flow areas within the plant during vegetative and productive growth periods [3,18,24]. Consequently, nitrogen accumulation, including that from fertilizer, is not significant in these organs. During the vegetative and productive cycle, fig trees develop new roots capable of absorbing water and mineral forms of nitrogen (N) from the soil. Some of this nitrogen can be assimilated into carbon chains and subsequently allocated to growing organs such as leaves and fruits [3,10].

Although higher percentages of accumulated nitrogen (N) were observed in annual organs in September, the stem exhibited the second highest percentage of N from fertilizer. It is desirable for perennial organs to serve as nitrogen accumulators, including those derived from fertilizers, as part of the nitrogen can be redistributed to other organs in the subsequent vegetative and productive cycle [25], reducing reliance on soil-applied nitrogen absorption within the same year. A potential reduction in nitrogen fertilizer application frequency or dosage in fig orchards [8,14] can be advantageous, decreasing fertilizer procurement costs and the risk of soil and water contamination in orchards.

However, regardless of the timing of supply, the N derived from fertilizer by the fig trees was less than 11%, indicating that more than 89% of the N contained in the organ tissue was derived from sources of N other than the fertilizer. This low percentage of N derived from the fertilizer in the fig trees has likely several explanations: it may be partially attributed to (i) volatilization of NH₃-N of the fertilizer applied on the soil surface and to volatilization of NH₃-N from the fig tree leaves throughout [5]; (ii) to leaching and runoff of mineral N, especially in the form of NO₃⁻-N [17,26]. However, it is believed that in the present study, transfer of N by leaching was less than the quantity of runoff from the soil surface because the percentages of N derived from fertilizer detected up to 0.20 m were small (Table 4); (iii) the N₂O-N denitrification in micropores of the soil saturated with water in the location of fertilizer application [27]; (iv) the possible small quantity of younger, white roots, which are responsible for the greater quantity of N taken up, in the area that received application of the nitrogen fertilizer [16]; (v) the availability of other sources of (unlabeled) mineral N in soil, such as mineralization of soil organic matter, but also mineralization of other plant litter, like senescent leaves, pruned branches and even litter from other cover crop species deposited between the plant rows [28]; (vi) the ability of microorganisms in competing with plants for N uptake [29]; (vii) the presence of a strong physical process of adsorption of mineral N (NH₄-N) in soil [28]; or yet (viii) the N accumulation in the roots, which were not evaluated in the present study [16,30] (Figure 2).

In the soil, at both times of nitrogen application, the highest values of excess ¹⁵N atoms and nitrogen derived from fertilizer (Ndff) were observed in the 0–0.10 m layer. This result may be attributed to the replacement of unenriched inorganic nitrogen by the applied nitrogen (enriched with ¹⁵N), which can be adsorbed onto functional groups of reactive inorganic soil particles or incorporated into microbial biomass or organic compounds within the soil [31,32].

This study elucidated the fate of nitrogen applied via soil, considering the recommended dose for fig cultivation and two growth and cell division periods. However, further studies are warranted to calibrate more effective doses and increase the application times according to fig tree phenological stages.

5. Conclusions

The annual organs of the fig tree, including leaves, fruit, and young shoots, exhibited the highest accumulation of N from soil application at both timings, with similar N uptake and accumulation levels. However, nitrogen fertilization had a minimal contribution to the overall nitrogen content of young trees.

Therefore, an installment of N doses during the growth and production cycle of fig trees, rather than a single application, can enhance nitrogen utilization from the fertilizer, potentially minimizing nitrogen loss and optimizing fertilizer efficiency.

Understanding the fate of nitrogen derived from fertilizer within the fig tree’s organs will allow for more precise adjustments when recommending nitrogen doses.