Impact of Nutrient Omissions on Growth and Biomass Nutrition in Young Plants of Cupuaçu Tree (Theobroma grandiflorum (Willd. ex Spreng.) Shum)

Abstract

Purpose

This study aimed to evaluate the growth, morphological changes, and mineral composition of young Cupuaçu plants subjected to the missing element technique in dystrophic Yellow Latosol.

Methods

The experimental design was completely randomized with ten treatments: control (macro + micronutrients), without nutrient application, and individual omission of N, P, K, Ca, Mg, S, B, Zn, in five replications. The nutrients concentrations, nutrients accumulations, and nutrient use efficiency were determined, and visual symptoms, growth biometrics, and plant biomass were measured.

Results

Nutrient concentration (-50.43% of N, -24.03% of P, -29.61% of K, -64.22% of Ca, -57.65% of Mg, -65.08% of S, -47.37% of B) and accumulation (-58.66% of N, -55.56% of P, -46.73% of K, -73.21% of Ca, -68.42% of Mg, -66.67% of S, -52.15% of B) were reduced by individual nutrient omissions compared to the control, causing changes in the morphology and coloration of the leaf blade, except for Zn. Plant height, number of leaves, and leaf area were reduced in all individual omissions, resulting in biomass loss in leaves, roots, stems, and total, except for Zn. Total biomass production in young Cupuaçu plants was most restricted by P, followed by Mg, K, Ca, S, N, and B. P deficiency affected the efficiency of utilization of all studied nutrients, but Zn omission did not affect nutrient use efficiency.

Conclusions

The results indicate that young Cupuaçu plants in dystrophic Yellow Latosol are sensitive to nutrient omission (N, P, K, Ca, Mg, S, and B), highlighting the need for efficient management in the cultivation system, as nutrient omissions can harm biometric parameters and dry mass production.

Introduction

The Amazon region boasts a high biodiversity of fruit species, with approximately 220 edible fruit-producing plant species, representing 44% of the native fruit diversity in Brazil (Neves et al. 2012). Cupuaçu (Theobroma grandiflorum (Willd. ex Spreng.) Shum.) cultivation is common in small farms, employing family labor and often intercropped with other crops, thereby enhancing the quality of life for small farmers (Martim et al. 2013).

Cupuaçu fruits contain minerals, fibers—especially soluble fiber—vitamins, and various secondary compounds such as polyphenols (Salgado et al. 2011; Vriesmann and de Oliveira Petkowicz 2009). This plant grows naturally in the forests of southern and northeastern Amazonia in Brazil and northeastern Maranhão, and also in neighboring countries like Venezuela, Ecuador, Costa Rica, Colombia, and Peru (Silva et al. 2008).

The nutritional management of cultivated Amazonian species is poorly understood, with limited literature on these species (Costa et al. 2024c; Viégas et al. 2022a). New studies on nutritional demands and nutrient interactions are needed for the nutritional management of Cupuaçu, especially in the Amazon region, which has acidic soils with low natural fertility. The recommended soils for Cupuaçu cultivation are sandy-clay, deep, and well-drained for high crop production (Coelho et al. 2021). However, Amazonian soils have low nutrient availability (Costa et al. 2021, 2023; Silva et al. 2024), limiting Cupuaçu production, particularly after successive harvests without nutrient replenishment, depleting soil nutrient solutions (Chaves et al. 2020).

The omission diagnosis method, or the missing element technique, is used to determine the nutritional requirements of plants. In this method, plants are grown in field or greenhouse conditions, comparing a control treatment (with all nutrients) and various treatments each omitting one nutrient at a time (Moretti et al. 2011; Skrebsky et al. 2008). This method can identify which nutrients limit plant growth and nutritional status in any soil substrate (Skrebsky et al. 2008). The omission diagnosis technique can also provide semi-quantitative information about nutrients that may limit plant growth (Malavolta 2006). It can be correlated with the visual diagnosis method, helping to understand nutrient deficiencies in plant development. This method has proven useful in identifying and differentiating the appearance of nutritional disorder symptoms for all evaluated nutrients (Alves et al. 2019), providing practical field knowledge for diagnosing nutritional disorders and managing crop nutrition, such as for cupuaçu.

However, little is known about the nutritional disorders caused by different nutrients in cupuaçu, a widely cultivated tropical tree. Understanding the effect of nutrient deficiencies on the concentration of other nutrients, as well as their impact on growth and morphological traits in cupuaçu progeny grown in medium-textured Yellow Latosol, is crucial for improving the nutritional management of the crop. This knowledge will play a significant role in enhancing plant performance and yield, contributing to the sustainable cultivation of this important species. In this context, it is relevant to evaluate the following hypotheses: (i) that macronutrient deficiencies alter the nutrient accumulation rate and nutrient use efficiency in cupuaçu plants, and, if confirmed, (ii) that the intensity of nutrient deficiency symptoms will vary depending on the specific nutrient omitted, directly affecting the growth and biomass accumulation of cupuaçu plants in dystrophic Yellow Latosol.

Therefore, this study aimed to evaluate the growth, morphological changes, and mineral composition of Cupuaçu plants (Progeny 32) cultivated using the missing element technique in medium-textured Yellow Latosol substrate under greenhouse conditions.

Materials and Methods

Study Location and Climatic Conditions

The study was conducted at Embrapa Amazônia Oriental, in a greenhouse located in the municipality of Belém-PA (01º27’21” S and 48º30’16” W), Brazil. The substrate used was medium-textured Dystrophic Yellow Latosol, at a depth of 0 to 20 cm, characterized by low natural fertility, deep and well-drained. Before setting up the experiment, a chemical and granulometric analysis of the soil was performed (Table 1), following Donagema’s methodology (2011) (Donagema et al. 2011). The genetic material used in the experiment was a bi-composite hybrid from the crossing of parents in the Cupuaçu breeding program at Embrapa Amazônia Oriental, using Progeny 32 from this process, with ancestry 174 × 186, originating from a mother in Coari-AM (174) and a father in Codajás-AM (186).

Table 1. Chemical and Granulometric characterization of the substrate before the experiment installation

Depth	OM	P	K	Na	Al	Ca	Mg	pH	Sand	Silt	Clay
Cm	g kg− 1	….mg dm− 3……….			……cmolc dm− 3……….			H2O	……. g kg− 1…………
0–20	13.84	5.00	10.00	4.00	1.50	0.20	0.10	4.3	0.75	0.13	0.12

pH determined in water (1:2.5 ratio); P and K measured using the Mehlich-1 method; Ca²⁺, Mg²⁺, and Al³⁺ determined using the KCl method (1 M); H⁺Al³⁺ measured with calcium acetate at pH 7.0; Organic matter (OM) determined by the sodium dichromate method; S determined by turbidimetry

Experimental Design

The experimental design was completely randomized with 10 treatments in five replications. The treatments were: control (complete, without nutrient omission); omission of N (-N); omission of P (-P); omission of K (-K); omission of Ca (-Ca); omission of Mg (-Mg); omission of S (-S); omission of B (-B); omission of Zn (-Zn); and the treatment without nutrient application (NNA).

Conducting the Experiment

Sowing was carried out in seedbeds, and when seedlings reached an average height of 6 cm with the emergence of a pair of leaves, they were transplanted into black plastic bags (35 × 18 cm x 0.20 mm), with a capacity of 5 dm³ of air-dried sifted soil substrate (TFSA) passed through a 4 mm sieve. Two seedlings were planted per bag, and later thinned to one seedling for uniformity 45 days after sowing.

45 days after sowing, mineral fertilization was performed according to the treatments, based on the missing element technique, following recommendations for the crop in the Amazon (Viégas et al. 2020). Fertilizations containing nitrogen and potassium were split into three applications: the first at 45 days after sowing (33.33%), the second at 90 days (33.33%), and the third at 150 days (33.33%).

Plant collection occurred 300 days after sowing, separating them into leaves, petiole + stem, and roots. Samples were packed in paper bags and placed in a forced-air circulation oven at 65º C until constant mass was obtained. The samples were then weighed to determine dry mass production in the different parts of the Cupuaçu plants and subsequently ground in a Willey mill.

The determination of nitrogen was carried out by the sulfuric digestion method, distillation with NaOH (10 M), and titration with H₂SO₄ (0.025 M) (Tedesco et al. 1995). For P, K, Ca, Mg, and Zn, the nitric-perchloric digestion method was used, with readings by colorimetry for P and atomic absorption spectrophotometry for K, Ca, Mg, and Zn (Carmo et al. 2000). Sulfur was determined by the turbidity method and boron by dry digestion and reading with azomethine-H (Carmo et al. 2000).

Nutrient accumulation (NA) in the aerial part was calculated based on the content of N, P, K, Ca, Mg, S, B, and Zn in the aerial part and the dry mass of the aerial part:

From the contents of N, P, K, Ca, Mg, S, B, Zn, and the dry matter value, the accumulation of macronutrients and micronutrients in the shoots was calculated. The nutrient content of the shoots was multiplied by the dry mass of the shoots. Nutrient use efficiency was calculated as follows: (dry mass)² / nutrient accumulation in the shoots.

Nutrient use efficiency in the aerial part, which is the plant’s ability to convert absorbed nutrients into biomass (Siddiqi and Glass 1981), expressed as the square of dry mass divided by nutrient accumulation in the dry mass:

Nutrient deficiency symptoms were described and photographed throughout the experiment. At 300 days, biometric measurements were also taken, measuring plant height with a tape measure, stem diameter with a digital caliper, number of leaves by simple leaf count, and leaf area by the indirect method of measuring the length and width of the first and second fully expanded leaves (Venturieri 1995).

Statistical Analysis

Data from the variables were subjected to normality (Royston 1995) and homogeneity (Gastwirth et al. 2009), tests, followed by analysis of variance (p < 0.05). When significant, means were compared by Tukey’s test (p < 0.05). Analyses were performed using the Python programming language (version 3.9.7; Python Software Foundation). Hierarchical clustering of data was conducted using Euclidean distance, and cluster grouping was performed using the single linkage method, employing Python (version 3.9.7; Python Software Foundation) as a programming tool.

Results

Impact of Nutrient Omissions on Nutrient Concentrations in Cupuaçu Plants

The nitrogen (N) concentration was reduced in treatments without nutrient application (NNA) and in the omission of N (-N), while the highest concentration of this nutrient was observed in the control treatment (Fig. 1a). For phosphorus (P) concentration, reductions were observed in NNA and P omission (-P) treatments, while an increase in leaf P concentration was noted in the omission of magnesium (-Mg) and sulfur (-S) (Fig. 1b).

Fig. 1 [Images not available. See PDF.]

Foliar concentrations of N (a), P (b), K (c), Ca (d), Mg (e), S (f), B (g), and Zn (h) in young Cupuaçu plants subjected to the missing element technique in dystrophic Yellow Latosol. Different letters indicate significant differences at the 5% probability level according to Tukey’s test

Potassium (K) concentration was reduced in NNA and boron omission (-B) treatments, with the highest concentration observed in the control treatment (Fig. 1c). Calcium concentration was reduced in NNA and the omission of calcium (-Ca), magnesium (-Mg), boron (-B), and zinc (-Zn) (Fig. 1d). An increase in Ca concentration was noted in the potassium omission (-K) treatment (Fig. 1d). For Mg concentration, the largest reduction was observed in the omission of Mg, while the highest increase was seen in the omission of N (-N) and K (-K) (Fig. 1e).

NNA and sulfur omission (-S) treatments were the ones that most reduced sulfur (S) concentration in Cupuaçu plants, while the highest concentration was observed in the K omission (-K) (Fig. 1f). For boron (B) concentration, the greatest reduction was noted in the B omission (-B), while the highest concentration was observed in the omission of N and K (Fig. 1g). For zinc (Zn), the greatest reduction in concentration was seen in NNA, P omission, and B omission treatments, while the highest increase was noted in Mg and S omissions (Fig. 1h).

The isolated omission of nutrients was able to alter the nutrient concentration in Cupuaçu leaves (Fig. 2), indicating reduced nutrient availability in the soil solution.

Fig. 2 [Images not available. See PDF.]

Foliar concentrations of young Cupuaçu plants (Theobroma grandiflorum (Willd. ex Spreng.) Shum) with nutrient supply and omission

Impact of Nutrient Omissions on Leaf Nutrient Accumulation in Young Cupuaçu Plants

The leaf accumulation of N in young Cupuaçu plants was reduced in the omission of N, P, and NNA, while the highest accumulation of this nutrient occurred in the control treatment (Fig. 3a). For P accumulation, the omission of P and NNA were the most limiting conditions, while the omission of S, Zn, and the control condition showed the highest accumulation of this nutrient (Fig. 3b).

Fig. 3 [Images not available. See PDF.]

Foliar accumulations of N (a), P (b), K (c), Ca (d), Mg (e), S (f), B (g), and Zn (h) in young Cupuaçu plants subjected to the missing element technique in dystrophic Yellow Latosol. Different letters indicate significant differences at the 5% probability level according to Tukey’s test

The greatest reduction in K accumulation in Cupuaçu plants occurred in NNA and P omission. However, the highest K accumulation rates were observed in the control, S omission, and Zn omission treatments (Fig. 3c). For Ca accumulation, reductions were observed in NNA, P omission, Ca omission, and Mg omission, while increases in accumulation rates were noted in the K omission (Fig. 3d).

For Mg accumulation, the greatest reduction was seen in the Mg omission, and the highest accumulation rate was observed in the omission of N and K (Fig. 3e). For S accumulation, a decrease was observed in S omission and NNA, while an increase in accumulation rate was noted in the omission of N and K (Fig. 3f).

The omission of P, Mg, B, and NNA caused a reduction in B accumulation in Cupuaçu plants, while the omission of N and S and the control condition increased the accumulation of this nutrient (Fig. 3g). For Zn accumulation, the lowest accumulation was observed in NNA, followed by P omission and B omission, while increases in Zn accumulation rates were seen in the omission of Mg and S (Fig. 3h).

Impact of Nutrient Omissions on Nutritional Symptoms in Cupuaçu Plants

N deficiency in Cupuaçu plants began with symptoms of color change from green to green-yellowish on the leaf edges (Fig. 4c). Additionally, it was observed that the tips and edges of the older leaves became necrotic. Finally, it was noted that N omission (-N) reduced the morphological characteristics of height compared to the control treatment (Fig. 4a).

Fig. 4 [Images not available. See PDF.]

Nutrient deficiency symptoms in young Cupuaçu plants subjected to the missing element technique in dystrophic Yellow Latosol

Fig. 5 [Images not available. See PDF.]

Nutrient use efficiency of N (a), P (b), K (c), Ca (d), Mg (e), S (f), B (g), and Zn (h) in young Cupuaçu plants subjected to the missing element technique in dystrophic Yellow Latosol. Different letters indicate significant differences at the 5% probability level according to Tukey’s test

Phosphorus deficiency symptoms altered the base of the leaf blade, reducing its base (Fig. 4d). P deficiency reduced plant size and, in older leaves, changed the coloration from green to dark green (Fig. 4d), compared to the control treatment. In Cupuaçu plants with K deficiency, marginal chlorosis was observed on the leaf blade, and in older leaves, the symptoms progressed to necrosis (Fig. 4e). K omission also reduced plant height (Fig. 6a). Ca deficiency altered the characteristics of the leaf blade between the veins, causing less roughness (Fig. 4f) and reducing plant height (Fig. 6a). In Mg omission, interveinal chlorosis followed by yellow spots that merged to form reddish margins was observed (Fig. 4g), along with a reduction in plant height (Fig. 6a).

Fig. 6 [Images not available. See PDF.]

Plant height (a), stem diameter (b), number of leaves (c), leaf area (d), leaf dry mass (e), stem dry mass (f), root dry mass (g), and total dry mass (h) of young Cupuaçu plants subjected to the missing element technique in dystrophic Yellow Latosol. Different letters indicate significant differences at the 5% probability level according to Tukey’s test

S deficiency in Cupuaçu plants did not express characteristic visual symptoms on the leaves; however, a reduction in the number of leaves was noted (Fig. 5c). In B omission, deformation of new leaves was observed, causing leaf apex curling, thickening, and necrosis at the leaf apex (Fig. 4h). In Zn-deficient plants, morphological changes in the leaf blade were observed, causing narrowing of the leaf blade and chlorosis on the edges of new leaves, progressing to necrotic spots (Fig. 4i). Zn deficiency also caused the formation of successive nodes with short internodes, forming small shoots in a rosette shape.

Impact of Nutrient Omissions on Nutrient use Efficiency in Cupuaçu Plants

N use efficiency was reduced by P and K omissions, while the highest use efficiency was observed in the omission of N and Zn (Fig. 5a). For P use efficiency, a decrease was noted in Mg omission and an increase in Zn omission (Fig. 5b). For K, use efficiency was reduced in P and Mg deficiencies, while the highest use efficiency was noted in B and Zn omissions (Fig. 5c).

Ca use efficiency was reduced by K omission and increased in B and Zn omissions in Cupuaçu plants (Fig. 5d). For Mg use efficiency, an increase was noted in Mg omission and a decrease in N, P, and K omissions (Fig. 5e). For sulfur, it was found that use efficiency was reduced in N, P, K, Ca, and Mg omissions and increased in S omission (Fig. 5f).

For B use efficiency, a decrease was noted in NNA and N, P, K, and Mg omissions, with the highest increase in B and Zn omissions (Fig. 5g). For Zn, the greatest decrease was observed in Mg omission, while the highest increase was noted in the control condition and B and Zn omissions (Fig. 5h).

Impact of Nutrient Omissions on Growth and dry mass Production in Cupuaçu Plants

Plant height was reduced in P, Mg, and NNA omissions, while an increase in height was noted in the control treatment and Zn omission (Fig. 6a). For stem diameter, the highest increase was observed in the control condition and N and P omissions, while the greatest reduction was seen in K, Ca, and Mg omissions, followed by NNA (Fig. 6b).

The highest number of leaves was observed in the control condition, while reductions were noted in N, P, K, Mg, S omissions, and NNA (Fig. 6c). Leaf area was also reduced in P, K, Ca, Mg, B omissions, and NNA, while an increase in leaf area was noted in the control condition and Zn omission (Fig. 6d).

P and NNA omissions were the most limiting conditions for leaf dry mass production, while the control condition and Zn omission showed the highest leaf dry mass production (Fig. 6e). For stem dry mass, the greatest reduction was seen in P, Mg, and S omissions, while an increase in stem dry mass was observed in the control condition and Zn omission (Fig. 6f).

The greatest reduction in root dry mass was noted in N, K, Mg, and S omissions, while the highest increase in root dry mass was seen in the control condition and B omission (Fig. 6g). For total dry mass, the greatest reduction was observed in P and Mg omissions, while the highest total dry mass was noted in the control condition and Zn omission (Fig. 6h).

Hierarchical Cluster Analysis of Response Variables in Cupuaçu Plants Cultivated with Different Nutrient Omissions

Hierarchical cluster analysis indicated the formation of three clusters: the first formed by the control treatments, B omission, and Zn omission; the second cluster formed by NNA, P omission, and Ca omission; and the third cluster formed by N, K, and S omissions (Fig. 7). The increase in N and K concentration, accumulation of N and K, stem diameter, number of leaves, and leaf area were associated with the control condition, while the increase in B concentration and accumulation of B and Mg was associated with N omission (Fig. 7).

Fig. 7 [Images not available. See PDF.]

Heat map of the hierarchical clustering with standardized data of concentrations, accumulations, nutrient use efficiency, and biometric and biomass measurements of young Cupuaçu plants subjected to the missing element technique in dystrophic Yellow Latosol. The colors in the heat map range from blue to red, indicating the strength and direction of the correlation, with blue representing a negative correlation and red representing a positive correlation. Values close to 1.0 or 0.0 indicate a strong positive or negative correlation, respectively, while values around 0.5 indicate little to no correlation

The decrease in K, Zn, and P concentration, accumulation of S, Ca, N, K, and Zn, and leaf area were associated with the NNA condition (Fig. 7). For P omission, the greatest association was observed with the decrease in N, K, S, and B use efficiency, total dry mass, and number of leaves (Fig. 7). Additionally, the decrease in Ca, Mg, and S use efficiency was associated with K omission, while the decrease in Ca concentration and accumulation was associated with Ca omission (Fig. 7).

Mg omission was associated with an increase in Mg use efficiency and P and Zn concentration, while S omission was associated with an increase in P accumulation, Zn accumulation, and S use efficiency (Fig. 7). For B omission, the greatest association was observed with an increase in B use efficiency and root dry mass, while Zn omission was associated with the highest N, P, K, Ca, and Zn use efficiency, P accumulation, plant height, and leaf dry mass (Fig. 7).

Discussion

The omission of nutrients in the cultivation of young Cupuaçu plants in dystrophic Yellow Latosol was able to reduce growth and dry mass production (Fig. 5), except for Zn omission. The results reveal the importance of nutrient management in the cultivation of young Cupuaçu plants, indicating that nutrient omissions reduce the performance of plants grown in dystrophic Yellow Latosol, leading to lower growth and biomass production.

The omission of N in Cupuaçu cultivation reduced the concentration of this nutrient in the leaves (Fig. 1a), reflecting lower absorption by the roots and consequently reducing N accumulation (Fig. 3a). The lower N accumulation in Cupuaçu plants led to a reduction in height, number of leaves, and leaf area, consequently reducing the dry mass production of leaves, roots, and total (Fig. 5). The reduced performance of Cupuaçu plants is associated with N deficiency in plant metabolism, impairing vital activities in the photosynthetic apparatus of plants (Prado 2021).

Plants subjected to N deficiency tend to reduce leaf area, as evidenced in this research (Fig. 5d), impairing CO₂ absorption and consequently reducing the photosynthetic efficiency of plants (Cruz et al. 2007). The presence of N is necessary for the production of amino acids, proteins, nitrogenous bases, nucleic acids, enzymes and coenzymes, vitamins, glycoproteins, and lipoproteins, as well as pigments (chlorophyll), as it is structurally part of these compounds (Prado 2021), Consequently, its deficiency hinders the synthesis of these organic compounds. The initial yellowing at the edges of the older leaves of plants under N deficiency is due to the redistribution of amino acids and the proteolysis of proteins, resulting in the collapse of chloroplasts and a decrease in chlorophyll content (Hörtensteiner and Feller 2002; Magalhães et al. 2023), consequently expressing N deficiency symptoms in older leaves (Fig. 4c).

When N deficiency affects CO₂ assimilation and transpiration in plants, it is due to the high mobility of this nutrient in the plant (Costa et al. 2024b; Taiz and Zeiger 2013). In its deficiency, N is easily redistributed in the form of amino acids via the phloem to new parts, especially young leaves and meristematic regions (Costa et al. 2024a), to minimize biological damage from this nutrient’s deficiency in new plant tissues. In this scenario, symptoms are initially visible in older leaves, consequently compromising the physiological functions of the younger leaves as well (Andrade and Boaretto 2019), which explains the visual symptoms in Cupuaçu seedlings (Fig. 4).

The omission of P in the cultivation of young Cupuaçu plants was the most limiting for total dry mass production (Fig. 5d), reducing plant growth (Fig. 4) and P accumulation (Fig. 3b). The omission of P reduced the nutrient concentration in the leaves (Fig. 1b) and consequently the P accumulation (Fig. 3b), due to lower availability in the soil solution, classified as low for Amazon soils (Brasil and Cravo 2020). This directly affected the efficiency of all nutrients (Fig. 5), highlighting its significant importance for nutrient balance in plants. Its absence causes substantial disturbances in plants, affecting nutrient interactions and consequently their development. Tropical soils are highly weathered, such as dystrophic Yellow Latosol, with high oxide concentrations, increasing P adsorption and reducing its availability in the soil solution for plant uptake (Hanyabui et al. 2020).

P deficiency reduces plant growth rates due to its biological function related to structural functions in plant cells and energy transfer and storage processes (Prado 2021). The omission of P reflects lower nutrient availability in plant metabolism, causing biochemical restrictions related to P functions (Malhotra et al. 2018). Additionally, some species under P deficiency may produce excess anthocyanins, giving leaves a slightly purple or dark green color (Taiz and Zeiger 2013). This occurs because P deficiency inhibits carbohydrate synthesis, increasing sugar levels and stimulating anthocyanin synthesis (Malhotra et al. 2018). In this scenario, P nutritional disorders cause biological damage to plant cells, potentially leading to significant biomass production losses and altering leaf coloration, as evidenced in our study (Fig. 4d).

The reduced growth of young Cupuaçu plants was also observed under K deficiency (Fig. 5). The low availability of K in the soil solution, classified as low (Brasil and Cravo 2020), restricted nutrient absorption by the plants, reflecting reduced leaf concentration (Fig. 1c) and consequently lower K accumulation (Fig. 3c). In this scenario, K management in Cupuaçu cultivation is essential to ensure greater growth and biomass production (Fig. 5). The low initial K concentration in the study soil (Table 1) was insufficient to meet the nutritional demands of Cupuaçu plants, highlighting that K management can be a limiting factor in Cupuaçu cultivation systems. In tropical soils, K is easily leached due to its low retention competitiveness on soil colloid surfaces, resulting in low availability for plants (White and Karley 2010; Zörb et al. 2014). Therefore, reinforcing the need for K supplementation in cultivation systems to improve plant performance.

The low amount of K absorbed by the plants is quickly redistributed from mature leaves to young ones, ensuring the formation of new tissues (Hafsi et al. 2014). In more mature tissues, such as older leaves, yellowing occurs, potentially progressing to necrosis at the edges of the leaf blade due to the accumulation of putrescine produced in the absence of K (Marques et al. 2004). In this scenario, K deficiency causes leaf color changes, leading to tissue death, as evidenced by symptoms in Cupuaçu leaves (Fig. 4e).

The results showed that K deficiency increased Ca and Mg concentrations in young Cupuaçu plants (Fig. 1d and e), as reinforced by hierarchical cluster analysis (Fig. 7). In the presence of K, the ion is preferentially absorbed by plants due to its monovalency and lower hydration compared to divalent Mg and Ca ions (Prado 2021). In this scenario, lower K supply increases the absorption of Ca and Mg in K-deficient plants. However, the higher absorption of these nutrients did not reduce the biomass production loss in young Cupuaçu plants.

Leaf Ca concentration was reduced with the omission of this nutrient in Cupuaçu cultivation (Fig. 1d), causing nutritional disturbances in plant metabolism, reducing growth and dry mass (Fig. 5). Ca concentration in Latosol is low, limiting nutrient supply to plants, as evidenced in the present study (Table 1) (Brasil and Cravo 2020). Calcium stabilizes the cell wall and cell membranes, regulates cation-anion balance, osmoregulation, and acts as a secondary messenger (Taiz and Zeiger 2013).

In the absence of Ca, nutritional disorders in plants cause leaf color changes, leading to new leaves with wrinkled and upward-curved edges with reticulated chlorosis throughout the blade (Fig. 4f). In this scenario, Ca management in the cultivation of young Cupuaçu plants is essential to ensure increased concentrations and accumulation (Figs. 1 and 3), enhancing plant growth and ensuring higher dry mass production (Fig. 5).

The omission of Mg also reduced dry mass in Cupuaçu plants (Fig. 5). The reduction in dry mass was also associated with lower Mg leaf concentration (Fig. 1e) and consequently lower nutrient accumulation (Fig. 3e). The reduced Mg leaf concentration is directly impacted by lower nutrient absorption, indicating the naturally low availability of this ion in the solution of tropical soils, such as dystrophic Yellow Latosol. In tropical soils, soil acidification induces increased retention of acidic cations on colloid surfaces, reducing colloid capacity to retain base cations such as Ca and Mg, consequently increasing ion leaching losses (Xiao et al. 2020). The loss of base cations like Ca and Mg reduces their availability to plants, consequently reducing nutrient uptake (Viégas et al. 2022b), as evidenced by reduced nutrient accumulation (Fig. 3d and f).

Lower Mg absorption by plants causes various metabolic disorders, as Mg plays several biochemical and structural roles in plants, including structural composition of chlorophyll and enzymatic activity (Prado 2021; Viégas et al. 2023a, 2024). Mg deficiency impairs chlorophyll synthesis, causing interveinal color changes in older leaves, as observed in this study in the interveinal areas of leaf margins (Fig. 4g). Therefore, Mg omission or inadequate management in the cultivation of young Cupuaçu plants can lead to growth loss and reduced biomass production, as evidenced in this research with a concentration of 0.1 cmol_c dm^− 3, indicating low availability (Brasil and Cravo 2020).

The omission of S in cupuaçu cultivation directly impacted the reduction of this nutrient’s leaf concentration (Fig. 1f), consequently decreasing S accumulation (Fig. 3f). Lower S accumulation in Cupuaçu plants causes metabolic disturbances, restricting vital plant activities, as S is part of amino acids such as cystine and methionine and contributes to protein stability (Prado 2021; Viégas et al. 2023b). Additionally, S is involved in enzymatic activity, metabolic reactions, and other compounds (Vitamin B₁). In this scenario, S is involved in various biochemical and physiological functions in plants, causing biological damage and biomass loss when omitted.

The biological damage from S deficiency in Cupuaçu plants caused reduced growth and biomass production (Fig. 5), but there was no significant leaf color change, indicating that this nutrient deficiency was not severe enough to alter leaf morphological characteristics.

Cupuaçu plants were also sensitive to B deficiency, reducing B leaf concentration and accumulation (Figs. 1 and 3). B deficiency resulted in leaf symptoms, indicating that nutritional disorders cause metabolic changes, including leaf color changes (Fig. 4h). B is directly involved in cell wall synthesis, membrane integrity, carbohydrate transport, reproductive growth, and cell elongation (Brdar-Jokanović 2020; Lewis 2019; Pereira et al. 2021).

In B-deficient plants, the accumulation and gene expression of specific transporters in the roots are modulated to ensure nutrient balance (Miwa and Fujiwara 2010). This strategy may have contributed to preventing root dry mass reduction in B omission (Fig. 5c), but it was not sufficient to mitigate aerial part damage (Fig. 5a and b). Efficient B management is essential for the good development of young Cupuaçu plants, as its absence can hinder growth and dry mass production in the aerial part.

The omission of Zn reduced leaf concentration of this nutrient in young Cupuaçu plants; however, the leaf concentration was above 40 mg kg^− 1, the minimum recommended concentration for most Amazonian crops (Veloso et al. 2020). In adult Cupuaçu plants cultivated in Yellow Latosol, a Zn concentration of 22 mg kg^− 1 was found (Viera 2021), lower than the values obtained in this study. In this scenario, the results indicate that in dystrophic Yellow Latosol, soil organic matter (SOM) can meet Zn nutritional demands, making it not a limiting factor in the cultivation of young Cupuaçu plants. Therefore, Zn deficiency resulted in dry mass production similar to the control treatment (Fig. 5d). Additionally, Zn availability is higher in acidic soils, as pH can affect this nutrient’s availability (Dechen et al. 2018; Viegas et al. 2021). In Brazilian tropical soils, low Zn availability was observed in Yellow Latosol (Singh and Moller 1984), but the results of this study differed from the literature, showing sufficient Zn in young Cupuaçu plants. This is corroborated by Zn use efficiency (Fig. 6h), and Zn omission did not affect N, P, K, Ca, B, and Zn use efficiency, demonstrating that this soil had sufficient Zn for plant metabolism without affecting the efficiency of the aforementioned nutrients. Further studies on Zn dynamics in Cupuaçu cultivation are still needed to understand this nutrient’s impact on crop sustainability.

Conclusions

The results demonstrate that young Cupuaçu plants (Progeny 32) are sensitive to the omission of nutrients (N, P, K, Ca, Mg, S, and B) when cultivated in dystrophic Yellow Latosol, indicating the need for efficient management in the cultivation system. The omission of these nutrients can cause growth and nutritional state impairments in the plants, leading to visible deficiency symptoms. Total dry mass production of young Cupuaçu plants was most severely restricted by P omission, followed by Mg, K, Ca, S, N, and B omissions. P deficiency affected the efficiency of utilization (NUE) of all studied nutrients, whereas Zn omission did not impact NUE. Although dystrophic Yellow Latosol has low natural fertility, nutrient supplementation allows for the cultivation of Cupuaçu plants, ensuring adequate growth and excellent biomass production performance.

Acknowledgements

The authors thank the study group on plant nutrition and soil fertility of the Amazon (GENFA) at the Federal Rural University of the Amazon, Capanema Campus, as well as the Brazilian Agricultural Research Corporation - Eastern Amazon and São Paulo State University UNESP/FCAV.

Author Contributions

BCS, IJMV, DASS and MGC conducted the experiment and wrote the primary version of the manuscript. JOC, RMA and BCS contributed to the data analysis and graph plotting. All authors contributed to the review of the manuscript. The design, administration and fundraising of the experiment was carried out by IJMV, MGC, DASS and JOC.

Data Availability

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Declarations

Competing Interests

The authors declare that they have no conflict of interest.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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