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Article

Nutrient Ratios in the Leaves and Stems of Eucalyptus and Corymbia Species Under High Soil Phosphate

by
Paulo Mazzafera
,
Rafaela Gageti Bulgarelli
,
Franklin Magnum de Oliveira Silva
and
Sara Adrián López de Andrade
*
Department of Plant Biology, Institute of Biology, University of Campinas, Campinas 13083-970, SP, Brazil
*
Author to whom correspondence should be addressed.
Forests 2025, 16(6), 869; https://doi.org/10.3390/f16060869
Submission received: 10 April 2025 / Revised: 14 May 2025 / Accepted: 21 May 2025 / Published: 22 May 2025
(This article belongs to the Section Forest Soil)
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Abstract

:
Eucalypts are a diverse group of Myrtaceae native to Australia and adapted to a wide range of edaphoclimatic conditions, including variation in phosphorus (P) soil availability. While Corymbia and Eucalyptus species have evolved in P-poor soils, they still respond to P additions. Nutrient ratios have been used to study nutritional imbalances in plants, as they relate to nutrient homeostasis within cells and ultimately productivity. This study investigated the effects of providing adequate (normal) and high doses of phosphorus (P) on nutrient ratios in leaves and stems of Eucalyptus and Corymbia species. High soil P may happen due to high natural soil concentration and over-fertilization. These species were pre-selected from a 22-eucalypt species screening, based on their responses—either positive, negative, or neutral—to increased dry mass at high soil P compared to normal P. Two species, Corymbia citriodora and C. maculata, which showed increased dry mass under high P levels, exhibited enhanced shoot growth and improvements in parameters related to photosystem efficiency. Except for Zn, which has an antagonistic relationship with P, the concentrations of other nutrients known to exhibit either antagonism or synergism with P were not significantly altered in the leaves and stems. As a result, there were no notable changes in the ratios with high P data compared to those with normal P data. Ratios calculated among K, Ca, Mg, Fe, and Mn data also remained unchanged. However, a principal component analysis, which was performed with all nutrient ratios, effectively separated the normal P and high P treatments and distinguished between species belonging to the genera Corymbia and Eucalyptus. The validity of such nutrient ratios is discussed, and it is suggested that they may not be applicable in studies involving high nutrient doses, which may also be true for other nutrients. Additionally, using ratios under unbalanced field fertilization may lead to an incorrect nutritional interpretation.

1. Introduction

Homeostasis in physiology is the process by which biological systems maintain internal stability and balance in response to external changes. It involves regulating various factors such as temperature, pH, ion concentration, and metabolites and nutrient levels to ensure optimal cellular function and the organism’s survival. Rather than a static state, homeostasis represents a dynamic equilibrium, characterized by continuous adjustments to meet ongoing changes [1].
In plants, homeostasis is closely linked to adaptability. They must adjust their physiological processes in response to various stimuli, particularly stresses from abiotic and biotic sources. Nutrient homeostasis in plant cells involves the regulation and balance of nutrient concentrations to maintain optimal physiological functions and growth [2]. This concept is crucial for understanding how plants manage nutrient uptake, transport, storage, and utilization, ensuring levels to support metabolic processes and promote healthy growth and yield. Consequently, improving crop yields and quality relies on balanced nutrient fertilizations that enhance plant growth and significantly boost crop productivity [3], ultimately contributing to cellular homeostasis.
Nutrient concentrations in plant tissues reflect processes such as nutrient uptake and remobilization and plant growth, and are influenced by species, soil fertility, mycorrhizal association, and environmental conditions [4,5]. Nutrient stoichiometry in plants refers to the study of the balance and ratios of nutrients and elements essential for optimal growth and development [6]. It highlights the relative quantities of macronutrients and micronutrients required for effective plant functioning. Some authors argue that critical nutrient ratios better reflect nutritional status and balance than nutrient concentrations, as they are less affected by growth dilution effects and aging processes [7]. Nutrient ratios in plant tissues have been extensively used to diagnose mineral imbalances in crops. However, as noted by [8], nutrient ratios in plant tissues are merely a numerical representation of their relative proportions and do not provide information about their actual concentrations. Furthermore, while nutrient ratios have been correlated with yield in some crops, this relationship has not been observed by others.
Phosphorus (P) is an essential macronutrient for plants, playing several vital roles in their growth and development [9]. While recommendations for P soil levels typically do not exceed 10–20 mg kg−1 for most crops [9,10,11], Brazil has seen high rates of P fertilization in various crops, resulting in soil P concentrations exceeding these levels. Given that P is strongly retained in weathered tropical soils, and the term “P soil legacy” has been used to describe soils with high P concentrations over years of successive P fertilization, this P is often chemically unavailable for plant uptake [12]. Notably, P toxicity is rarely observed under field conditions [13], and some eucalypt species are especially sensitive to P at an elevated soil P availability [14]. Certain crops, such as garlic, continue to respond positively to productivity even at soil P levels exceeding 500 µM [15,16].
Eucalypts are an economically significant crop in Brazil, with applications in wood production, timber, and the pharmaceutical and chemical industries [17,18]. Native to the Australian continent, eucalypts are naturally adapted to environments with low or very low P availability [19]. These environmental conditions have led to the development of several physiological mechanisms that enable these plants to thrive under P deficiency [20,21]. Species from the genera Corymbia and Eucalyptus are the most widely planted hardwood trees due to their desirable agronomic traits and the industrial relevance of their products [22,23].
In this study, we investigated growth, physiological responses, and nutrient stoichiometry in leaves and stems of eucalypt species from Eucalyptus and Corymbia grown at two contrasting soil P levels: the recommended level (7.7 mg kg−1) and a higher level (45.3 mg kg−1). We anticipated that increasing the soil P availability to nearly six times the recommended concentration would induce noticeable changes in biomass accumulation, photosynthesis-related traits, and nutrient concentrations and ratios. We also anticipated differences in foliar and stem nutrient ratios between species of the two studied genera.

2. Material and Methods

2.1. Experimental Design

The experiment was conducted in a greenhouse using a 6 × 2 factorial design, which included 6 eucalypt species and 2 P levels, with 5 replicates for each treatment. The P levels were categorized as normal (7–10 mg kg−1 of available P) and high (45 mg kg−1 of available P). Available P refers to the soil resin-extractable phosphate, which is considered the soil fraction accessible for plants.

2.2. Soil Sampling and Treatment

A mixture of soil and coarse sand in the proportion 1:1 (v:v) was used as a substrate for the cultivation of eucalypts. The soil used was a sample of an Oxisol [24] collected from the 20 to 60 cm layer in Campinas region, São Paulo (Brazil). The original soil sample was chemically characterized (Table 1), and according to the results obtained in the fertility analysis, the P concentrations necessary to reach the desired P levels were calculated, and the concentrations of Cu, Mg, Zn, Mn, and B were adjusted as recommended for forest species [10]. The following amounts of nutrients were added in mg kg−1 of soil: B (H3BO3) 2.25, Cu (CuCl2) 2.7, Mn (MnSO4) 15.6, Zn (ZnCl2) 52.7, and Mg (MgSO4) 418.31. To reach the previously established P levels, P was added as KH2PO4. The mixture of sand and soil was made in a concrete mixer, and during the process, aqueous solutions containing the salts were added slowly. After homogenization, the substrate was reserved in 1000 L tanks for 30 days at ambient temperature, to allow phosphate to react with the soil [25]. After this period, a new chemical analysis of the soil was performed (Table 1). The available P in the soil and exchangeable bases Ca, K, and Mg were determined by the ion-exchange resin method [26]. Boron was extracted with hot water and metal micronutrients with 0.005 mol L−1 DTPA solution at pH 7.3. The nutrient concentrations in the extracts were determined by inductively coupled plasma-optical emission spectrometry (ICP-OES; JobinYvon, JY50P Longjumeau, France). Soil pH was determined in CaCl2. Sufficient levels, herein named normal P, reached 7.7 mg P kg−1 soil and high P, 45.3 mg kg−1 soil. The normal P level ranged within the adequate range of available soil P for eucalypt plantation in Brazil, and the high P level was above the lower limit values for high soil P concentrations for this crop [10].

2.3. Plant Material

The species used in this study were selected based on a preliminary screening of 22 species cultivated under two soil P levels, normal and high, in 5 L pots and grown in a greenhouse for nine months. After this growth period, plants were collected, and total plant dry mass was determined in five replicates per species (Figure 1). Six species were selected based on their biomass accumulation under high P and normal P levels, i.e., two species which had increased dry mass accumulation, two with decreased accumulation, and two which had little change in dry mass accumulation. Eucalyptus henryi (S.T. Blake) K.D. Hill & L.A.S. Johnson and E. urophylla S. T. Blake were chosen because they exhibited a reduced biomass production at the high P level compared to the normal P level (mean dry mass at high P minus mean dry mass at normal P). E. microcorys F. Muell. and E. resinifera Sm. were selected for their similar biomass production under both P levels. Corymbia citriodora (Hook.) K.D. Hill & L.A.S. Johnson and C. maculata (Hook.) K.D. Hill & L.A.S. Johnson were chosen due to their higher biomass production at a high P level.
Seeds of these eucalypt species were obtained from clonal gardens of Caiçara Sementes (Brejo Alegre, São Paulo, Brazil) and the Institute of Forest Research and Studies (IPEF, Piracicaba, São Paulo, Brazil). Seeds were germinated in a commercial substrate, and after two months, seedlings were transferred to 5 L pots containing soils with either high or normal P levels. Plants were irrigated with tap water and received additional nitrogen fertilization with urea, which totaled 200 mg of N per pot. Plants were grown in a greenhouse for nine months, under average maximum and minimum temperatures of 38.9 °C and 19.2 °C, respectively. The photoperiod ranged from 12 to 10 h of light per day, with a maximum photon flux density of 1800 μmol m−2 s−1.

2.4. Photosynthesis-Related Parameters

One week before plant collection, photosynthesis and stomatal conductance were obtained using an infrared gas analyzer (LI 6400, LI-COR, Lincoln, NE, USA), setting the equipment to ambient CO2 concentration (~400 ppm) and 1000 μmol photons m−2 s−1. A portable fluorimeter (FluorPen FP100, Photon Systems Instruments, Czech Republic) was used to obtain the potential quantum efficiency (Fv/Fm) and non-photochemical quenching (NPQ) in dark-adapted leaves. Fv/Fm was calculated as (Fm-Fo)/Fm, where Fo is the minimum fluorescence yield and Fm is the maximum fluorescence yield under dark-adapted conditions. NPQ was calculated as (Fm − Fm’)/Fm’, where Fm’ is the maximum fluorescence yield under light-adapted conditions. For light-adapted leaves, the effective quantum yield of photosystem II (ФPSII) was determined. These measurements were made in the first fully expanded leaves from the top to the bottom, between 9 h and 14 h. To calculate the photosystem II energy index, Fv/Fm and NPQ values were used and calculated as [Fv/Fm − NPQ]/Fv/Fm.

2.5. Growth Parameters and Nutrient Analysis

Plant height and stem diameter (5 cm from the soil) data were obtained at the end of the experiment. Plants were then separated into stems, leaves, and roots (washed under running tap water) and dried at 60 °C for 20 days. Dried leaves and stems were sent to a private laboratory (Pirasolo Laboratório Agrotécnico Piracicaba Ltd.a, Piracicaba, São Paulo, Brazil) for nutrient analysis by ICP-OES, except for N, which was determined using the Kjeldahl method [27].

2.6. Statistical Analysis

All data represent the means of five biological replicates. Data sets were tested for homogeneity of variances before the analysis of variance (two-way ANOVA). Then, the effect of soil P availability was analysed separately for each species using a one-way ANOVA, and means were compared using Tukey’s test (p < 0.05), using SISVAR software [28]. Principal component analysis (PCA), based on the covariance matrix of normalized data, was conducted using the nutrients/P ratios to identify which variables best explained the separation of species based on a dry accumulation at the high P level. The first two components were retained for interpretation. PCA was performed using Minitab 17 software (Minitab Inc., Shanghai, China).

2.7. GenAI Usage

Generative ChatGPT, version GPT-4 (Large language model: https://chat.openai.com/, accessed on 15 April 2025) was used to review and correct English grammar, spelling, and language clarity during manuscript preparation. No content was generated or written by the AI, and all scientific interpretations, data analyses, and conclusions were solely produced by the authors.

3. Results

Plants grown under normal P levels did not exhibit typical deficiency symptoms, such as purplish pigmentation associated with anthocyanin accumulation, indicating that the available P in the soil was sufficient to support normal metabolic functions in all 22 species initially evaluated (Figure 1).
The distribution of dry mass among stems, leaves, and roots reveals distinct allocation patterns in the six selected species. C. citriodora and C. maculata accumulated the highest total dry mass under high P conditions (Figure 2A). Specifically, C. citriodora displayed a greater stem mass (Figure 2C) compared to its leaf mass (Figure 2B). In contrast, C. maculata showed a tendency to accumulate more mass in its leaves than in its stems. In both species, root biomass had a minimal effect on soil P levels and did not contribute to the increase in the overall biomass observed in plants under high P levels (Figure 2D). Conversely, E. urophylla and E. henryi exhibited reduced growth under high P levels. The reduction in dry mass observed in E. urophylla was primarily due to a significant decrease in root mass (Figure 2D). In E. henryi, the reduction in total dry mass may be attributed to discrete decreases in both leaf and stem biomass (Figure 2B,C). E. microcorys and E. resinifera were not significantly affected by P supply levels (Figure 2D).
In general, plant dry mass, height, shoot dry mass, and stem diameter were higher in C. citriodora and C. maculata plants growing at a high P level (Figure 3A–D). The most pronounced biomass increase was observed in C. maculata, which produced 145% more total biomass under high P levels compared to normal P levels. C. citriodora also showed a significant increase, with 60% higher biomass under high P levels (Figure 3A).
Despite some differences observed between plants grown under normal and high P conditions, photosynthesis-related parameters such as stomatal conductance (gs) and ФPSII did not effectively explain the variation in total dry mass accumulation among species (Figure 4B,C). However, it is interesting to observe that Fv/Fm showed an inverse pattern to that of NPQ in C. citriodora and C. maculata, i.e., while Fv/Fm was higher in plants grown at high P levels, NPQ was 35% lower than that under normal P levels (Figure 4). When using these two parameters to calculate the photosystem energy index, which better reflects the balance between photochemical efficiency and energy dissipation, it was found that plants grown under high P levels generally exhibited similar values compared to those grown under normal P levels. However, C. citriodora and C. maculata showed around 66% lower photosynthesis energy indices under high P conditions (Figure 4F).
Except for E. henryi, a higher soil P availability led to increased P concentrations in both leaves and stems (Figure 5B). In most species, P concentrations were similar in the leaves and stems of each genotype, with some exceptions, such as E. henryi and E. microcorys plants that accumulated more P in the leaves grown in soil with high P levels. The highest concentrations of K were observed in the leaves of E. citriodora and E. maculata (Figure 5C). Differences in K concentrations between P treatments were relatively limited, but significant effects were observed in the leaves of E. urophylla and E. microcorys, and the stems of C. henryi (Figure 5C). Regarding Ca, concentrations were generally similar, except for leaves of C. henryi, E. urophylla, and E. microcorys, which showed slight variations (Figure 5D).
N and Mg concentrations were consistently higher in the leaves than in the stems in all species and P levels (Figure 5A,E). The highest concentration of N was found in the leaves of C. citriodora and E. urophylla. In leaves, N and Ca were the nutrients present in the highest concentrations, followed by K. In contrast, Ca was the nutrient found in the highest concentration in the stem, followed by K and N (Figure 5). Except for E. henryi, the increased availability of P in the soil resulted in higher concentrations of P in both leaves and stems (Figure 5B). Generally, P concentrations in the leaves and stems were similar within each genotype, although exceptions occurred, such as higher P concentrations in the leaves of E. henryi and E. microcorys grown in high P soil. The highest concentrations of K were observed in the leaves of C. citriodora and C. maculata (Figure 5C). A few differences regarding K concentrations were noted between P treatments, specifically in the leaves of E. urophylla and E. microcorys, as well as the stems of C. henryi. Additionally, except for the leaves of C. henryi, E. urophylla, and E. microcorys, Ca concentrations in leaves and stems were similar (Figure 5D).
Similar to N, Mg concentrations were higher in the leaves than in the stems across all species (Figure 5E). In general, the S concentration was higher in leaves than in the stems (Figure 5F). Interestingly, leaves and stems of C. citriodora had higher S concentrations under the normal P levels than under high P levels. There was no relationship between macronutrient concentrations and total dry mass production, which guided the classification of the six species into three distinct growth response groups.
Mn concentrations were consistently higher in the leaves compared to the stems across all species and soil P levels (Figure 6D). B concentrations also tended to be higher in the leaves, although with a few exceptions (Figure 6E). Although not statistically significant in all cases, a noticeable trend of reduced Cu concentrations in the stems of plants under high P was observed, particularly in C. henryi (Figure 6A). Conversely, Zn concentrations decreased in response to high P (Figure 6C). The highest concentrations of Fe and Zn were found in the leaves of C. citriodora, E. maculata, and E. henryi under normal P levels (Figure 6B,C). E. microcorys and E. resinifera exhibited the highest Mn concentrations in their leaves (Figure 6D). On average, Mn was the micronutrient found in the highest concentration in both leaves and stems.
In C. citriodora, E. urophylla, and C. henryi, a higher soil P availability was associated with a reduction in Zn concentrations in leaves and/or stems. Additionally, the higher soil P availability led to lower Mn concentrations in the leaves and stems of C. citriodora, C. henryi, and E. microcorys. No consistent correlation was observed between micronutrient concentrations and total dry mass accumulation, which supported the classification of the six species into three distinct response groups.
A high soil P availability resulted in a decrease in all macronutrients-to-P ratios in both leaves and stems (Figure 7). The N/P and Mg/P ratios were consistently higher in leaves compared to stems across all species and soil P levels (Figure 7A,E). Among the macronutrients, the highest ratios relative to P were observed for Ca, followed by N, as both Ca and N were present in the highest concentrations in leaves and stems (Figure 5A,D). In stems, K/P, S/P, and Ca/P were higher under normal P levels than under high P levels only in E. urophylla. No correlation was noted between macronutrient-to-P ratios and total dry mass accumulation, which led to the separation of the six species into three distinct response groups.
Numerically, in most species and in both tissues analyzed, the high soil P availability resulted in a decrease in the micronutrient-to-P ratios (Figure 8). The most significant differences were found for Mn/P and Zn/P ratios (Figure 8C,E). Overall, Mn/P and B/P ratios (Figure 8C,D) were consistently higher in the leaves than in the stems across all species and both P treatments. No correlation was found between micronutrient-to-P ratios and total dry mass accumulation, which led to the classification of the six species into three distinct response groups.
In general, the increased soil P availability resulted in minimal significant changes in the N/K, K/Ca, K/Mg, and Fe/Mg ratios (Figure 9). Among these, the K/Mg ratio is considered synergistic, whereas the others represent antagonistic nutrient relationships. The N/K ratio was consistently higher in the leaves compared to the stems (Figure 9A), which can be attributed to the higher N concentration observed in the leaves relative to the stems (Figure 5A). The K/Ca ratio increased in the leaves of E. urophylla, E. microcorys, and E. resinifera under high P levels in the soil (Figure 9B). In the stems, this ratio also increased in E. urophylla and E. resinifera, while a decrease was observed in E, microcorys. Significant changes in the K/Mg ratio were only observed in E. urophylla (Figure 9C). No correlation was found between these nutrient ratios and total dry mass accumulation, which led to the separation of the six species into three distinct response groups.
The PCA showed that the first (PC1) and second (PC2) components explained 52.4% and 17.5% of the total variation, respectively. The PCA based on all nutrient ratios identified four distinct groups (Figure 10). Two of these groups included all species grown under high P levels but were separated by genus: one comprised Corymbia species and the other comprised Eucalyptus species. The other two groups were comprised of plants grown under normal P levels in the soil, also separated by genus, with one group comprising Corymbia species and another comprising Eucalyptus species. The N/K ratios in leaves and stems contributed significantly to distinguishing Eucalyptus from Corymbia species under high P conditions. Under normal P conditions, the K/Mg, K/Ca and Fe/Mn ratios were associated with the separation between the two genera (Figure 10).

4. Discussion

4.1. Plant Growth and Photosynthesis Under Normal and High P Soil Conditions

In this study, 22 eucalyptus species were initially evaluated for biomass accumulation under normal and high P soil conditions. Based on their contrasting responses, six species were selected for further analysis: two exhibited an increased dry mass under high P conditions, two maintained similar dry mass levels, and two experienced a decrease in mass. Dry mass partitioning among leaves, stems, and roots showed different accumulation patterns among the selected species. In C. citriodora and C. maculata, the increase in total biomass under high P conditions was exclusively due to greater leaf and stem mass, accompanied by increases in plant height and stem diameter. In contrast, the two species that experienced reductions in total biomass under high P conditions showed different patterns: E. urophylla showed reduced root biomass, while C. henryi showed a decrease, mainly in leaf biomass.
A previous study using the same six species under recommended levels of P in the soil [10] showed a significant stimulation of shoot growth compared to P-deficient conditions [17]. Consequently, these findings suggest that species-specific responses differ significantly not only between low to sufficient P conditions, but also between sufficient and high P conditions. The differences in biomass allocation between shoots and roots indicate distinct physiological or metabolic mechanisms underlying P acquisition and utilization across species.
While some eucalypt species, such as E. marginata, are especially sensitive to high P concentrations in the soil [14], other plant species, like garlic, can still respond positively to excessively high P levels in the soil [16]. These contrasting responses highlight the role of species-specific mechanisms and the influence of soil characteristics in modulating plant responses to P availability. It has been suggested that at high P levels in the soil, plants may reduce the expression of root P transporters to mitigate the risk of P overaccumulation and toxicity [9]. Additionally, high P concentrations may disrupt mycorrhizal association functioning, leading to overall negative impacts on plants [29]. Our results, along with those from other studies, indicate that species respond differently to high soil P, leading to a higher accumulation of P in the leaves and increased dry mass and productivity. Thus, the understanding of toxic P levels should consider species diversity and require further investigation.
There was no relationship between photosynthesis and the increase in biomass production in C. citriodora and C. maculata grown under high P levels. However, these species showed a reduction in the NPQ and an increase in Fv/Fm under high P conditions. NPQ is a protective mechanism of the photosynthetic machinery, which dissipates excess light energy in the photosystems through heat [30]. The photosystem II energy index, which correlates negatively with energy dissipation in the photosystems [31], indicates higher plant efficiency under high P conditions, thus supporting the higher Fv/Fm observed in those species. The importance of P in the maintenance of photosystem structures is well known [32]. In cotton, P supply has been shown to enhance the photosystem capacity to dissipate excess energy and reduce the production of reactive oxygen [33]. Thus, it seems reasonable to infer that plants of C. citriodora and C. maculata grown under high soil P conditions, which led to a higher P concentration in leaves and stems, showed improved photosystem efficiency. The lack of a direct relationship between photosynthesis and changes in growth rate has been attributed to the complexity of carbon use efficiency, which depends on multiple factors that are not yet fully understood [34]. It has been shown that carbon use efficiency is influenced by changes in soil nutrient availability, which can modulate biomass partitioning by directing carbon to roots, wood, or leaves, or by allocating carbon to respiration, root exudation, or symbiont association, as strategies to adapt to nutrient availability and support growth.

4.2. Nutrient Concentrations and Ratios in Leaves and Stems

In our study, leaf P concentrations under normal P conditions were generally within the adequate range for eucalypts, and little exceeded these ranges under high P conditions [10]. Moreover, for some species, such as C. maculata, C. henryi, and E. microcorys, P concentrations double under high P conditions. In general, the nutrients found in the highest concentrations in the leaves of the six studied species were N, Ca, and K. While leaf N concentrations exceeded those in the stems, Ca and K were found in similar concentrations in both organs. In poplar, Fromm [35] showed that the highest stem K concentrations occur in the cambial zone and developing xylem. This K distribution in the stem seems to be associated with auxin localization, as auxin also accumulates in the cambium region [36]. This accumulation of auxin is related to stem morphogenesis, as well as the accumulation of non-structural carbohydrates for the synthesis of cellulose and other cell wall polymers [37]. These essential metabolic activities in the stem depend on adequate water availability in the stem [37] and the maintenance of tissue water status, a function closely linked to K in eucalypts and other forest species [38]. Concentrations of Ca in the stem have been associated with water consumption, as its uptake increases with increased transpiration rates [39]. Among the studied eucalypt species, C. maculata showed one of the highest stomatal conductance levels and also high Ca, K, and Mg concentrations in leaves and stems, which may be related to higher water consumption. Nonetheless, this association of Ca and K concentrations in stems and leaves and stomatal conductance does not occur for other species.
Fromm [35] also found high Ca concentrations in the stems of tree plants, but in this case, in the phloem. Ca is the most extracted nutrient by eucalypts, followed in descending order by N, K, S, Mg, and P [40]. Laclau et al. [41] also observed high Ca and Mg concentrations in the bark of eucalypts, noting that nutrient concentrations are generally higher in the bark than in other stem tissues [5]. In our study, leaves generally had higher Mg concentrations than stems. Notably, P concentrations increased in both leaves and stems of plants under high P levels, a pattern not observed for any other nutrient. Previous reports suggest that in eucalypts, the stem may function as a P storage organ [20,41].
The main micronutrients affected by high P availability in our study were Zn and Fe, both of which tended to increase in concentration in Corymbia species. Additionally, Mn and B were generally in higher concentrations in the leaves. Previous studies on various other crops have shown that elevated P levels can alter micronutrient concentrations [42,43], mainly Fe and Zn. These changes may result from altered solubility in soil, changes in root-to-shoot translocation, dilution effects due to increased biomass, or impacts on mycorrhizal associations [14,44]. The antagonistic effect of high P on Zn uptake and accumulation in plants can be due to a reduced translocation from the roots [44].
Nutrient ratios in plants have long been discussed as potential indicators of nutritional balance, thus driving fertilization practices [7]. Unlike nutrient concentrations, nutrient ratios are independent of plant mass. Some ratios have received more attention due to their proposed functional relevance, such as N/P, K/P, Mg/P, B/P, and Cu/P, which are often considered to be synergistic, and S/P, Fe/P, and Zn/P, which are seen as antagonistic [13]. In our study, for all eucalypt species except for E. urophylla, low N/P ratios under high P conditions were clearly below the accepted normal range, suggesting that growth was more limited by N [7]. Our data also showed that, with few exceptions, mostly Fe/P ratios, most macro and micronutrient ratios decreased in both leaves and stems under high soil P conditions, even among those nutrients considered synergic. Such a result is probably a consequence of the significant increase in P in the stem and leaves. Thus, as stated by Summer [8], a ratio between nutrient concentration in a plant tissue is merely a number representing their relative proportions and does not give any information about the actual concentrations in plant tissues. Here, even at high P levels, the concentration levels of Zn in the leaves were still in the appropriate range for eucalypts [10,45]. Therefore, nutrient ratios may have a practical significance when nutrient concentrations are in the range of deficiency or sufficiency.
The relationship between nutrient ratios, eucalypt species, and soil P levels was shown by the PCA (Figure 10). The K/Mg and K/Ca ratios in both stems and leaves, along with Fe/Mn ratio in stems, contributed to the separation between plants grown under normal versus high P conditions. Leaf ratios, especially Fe/P, K/P, Cu/P, Zn/P, and Fe/Mn, were particularly important to separate Corymbia species. This separation suggests that species respond differently to increased P availability. Considering the distribution of ratios in the upper PCA quadrants, stem nutrient data better explain the positioning of Eucalyptus species, while leaf data better explain the positioning of Corymbia in the lower quadrants. However, the nutritional significance of these results is obscure and difficult to interpret.
This study revealed species-specific differences in response to high P levels that may be driven by a combination of physiological mechanisms, including different patterns of biomass partitioning, the differential regulation of photosynthetic efficiency, and distinct nutrient uptake and allocation strategies. Nutrient stoichiometry, particularly reduced N/P and micronutrient/P ratios under high P levels, further suggests imbalances that may constrain growth despite increased P availability. These results emphasize that eucalypt species exhibit diverse physiological adaptations to soil P availability, with implications for species selection and fertilization management.

5. Conclusions

Our results indicate a substantial variation among eucalypt species in their response to increased P availability in the soil. This variation was evident not only in total plant dry mass accumulation but also in the distribution among leaves, stems, and roots. All six species investigated showed increased P concentrations in their leaves and stems under high P conditions. In young eucalypt plants, elevated P levels generally led to positive or neutral effects on biomass production and improvements in photochemical parameters. However, the use of high P rates should be approached with caution, as nutrient-to-phosphorus ratios indicated potential nutritional imbalances, underscoring the need for balanced nutritional management.
Nutrient-to-P ratios, for both macronutrients and micronutrients, did not indicate consistent synergistic or antagonistic interactions, except for Zn, whose concentration in leaves and stems decreased with increasing P levels. Other nutrients typically considered antagonistic to P, such as K, Ca, Cu, and Fe, did not exhibit reduced concentrations. Similarly, the expected synergistic relationship between Mg and P was not confirmed. These findings suggest that nutrient ratios may have limited diagnostic value for identifying nutritional imbalances when plants are grown under higher nutrient availability, indicating a need for further testing with other nutrients.

Author Contributions

Conceptualization, S.A.L.d.A. and P.M.; formal analysis, P.M., F.M.d.O.S. and S.A.L.d.A.; funding acquisition, P.M. and S.A.L.d.A.; investigation, P.M., R.G.B., F.M.d.O.S. and S.A.L.d.A.; supervision, P.M. and S.A.L.d.A.; writing, P.M. and S.A.L.d.A. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the São Paulo Research Foundation (FAPESP—Grant number 2016/25498-0).

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.

Acknowledgments

We thank FAPESP, CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil), and Conselho Nacional de Desenvolvimento Científico e Tecnológico—Brasil (CNPq) for post-doctoral, doctoral, and research fellowships to FMdOS (Grant number 2018/09624-0), RGB, and PM, respectively. We thank ChatGPT (GPT-4, OpenAI) for assistance with the English language editing of this manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Difference in total plant dry mass production between eucalypt plant species grown in soils with high and normal P levels. Values represent the result of subtracting total dry mass of plants grown under normal P levels (7.7 mg kg−1) from those grown under high P levels (45.3 mg kg−1). Positive values indicate higher biomass under high P levels, negative values indicate reduced growth, and values near zero indicate similar growth across P levels. Selected species with reduced biomass accumulation at the high P level compared to the normal P level are shown in red, those with similar biomass production under both P levels are shown in yellow, and those with higher biomass production at the high P level are shown in green.
Figure 1. Difference in total plant dry mass production between eucalypt plant species grown in soils with high and normal P levels. Values represent the result of subtracting total dry mass of plants grown under normal P levels (7.7 mg kg−1) from those grown under high P levels (45.3 mg kg−1). Positive values indicate higher biomass under high P levels, negative values indicate reduced growth, and values near zero indicate similar growth across P levels. Selected species with reduced biomass accumulation at the high P level compared to the normal P level are shown in red, those with similar biomass production under both P levels are shown in yellow, and those with higher biomass production at the high P level are shown in green.
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Figure 2. Total (A), leaf (B), stem (C), and root (D) dry masses of Eucalyptus and Corymbia species grown under high and normal P levels in the soil.
Figure 2. Total (A), leaf (B), stem (C), and root (D) dry masses of Eucalyptus and Corymbia species grown under high and normal P levels in the soil.
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Figure 3. Plant dry mass (A), height (B), shoot dry mass (C), stem diameter (D), and root dry mass (E) in Eucalyptus and Corymbia species grown under normal (light gray) and high (dark gray) P levels in the soil. Asterisks indicate significant differences between P treatments for each species (Tukey test, p < 0.05). Bars represent standard error (n = 5).
Figure 3. Plant dry mass (A), height (B), shoot dry mass (C), stem diameter (D), and root dry mass (E) in Eucalyptus and Corymbia species grown under normal (light gray) and high (dark gray) P levels in the soil. Asterisks indicate significant differences between P treatments for each species (Tukey test, p < 0.05). Bars represent standard error (n = 5).
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Figure 4. Photosynthetic parameters in Eucalyptus and Corymbia species grown under normal (light gray) and high (dark gray) phosphorus (P) levels: net photosynthesis rate (A), effective quantum yield of photosystem II (ФPSII) (B), stomatal conductance (gs) (C), non-photochemical quenching (NPQ) (D), potential quantum efficiency (Fv/Fm) (E), and photosystem energy index (F). Asterisks indicate significant difference between P treatments within each species (Tukey test, p < 0.05). Bars represent standard error (n = 5).
Figure 4. Photosynthetic parameters in Eucalyptus and Corymbia species grown under normal (light gray) and high (dark gray) phosphorus (P) levels: net photosynthesis rate (A), effective quantum yield of photosystem II (ФPSII) (B), stomatal conductance (gs) (C), non-photochemical quenching (NPQ) (D), potential quantum efficiency (Fv/Fm) (E), and photosystem energy index (F). Asterisks indicate significant difference between P treatments within each species (Tukey test, p < 0.05). Bars represent standard error (n = 5).
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Figure 5. Macronutrient concentrations, nitrogen (A), phosphorus (B), potassium (C), calcium (D), magnesium (E) and sulfur (F), in leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels in the soil. Green (leaves) and brown (stems) asterisks shown next to the bars for the normal P treatment indicate significant differences between P treatments within each species and in each tissue (Tukey test, p < 0.05). Bars represent standard error (n = 5).
Figure 5. Macronutrient concentrations, nitrogen (A), phosphorus (B), potassium (C), calcium (D), magnesium (E) and sulfur (F), in leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels in the soil. Green (leaves) and brown (stems) asterisks shown next to the bars for the normal P treatment indicate significant differences between P treatments within each species and in each tissue (Tukey test, p < 0.05). Bars represent standard error (n = 5).
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Figure 6. Micronutrient concentrations, copper (A), iron (B), zinc (C), manganese (D) and boron (E), in leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels in the soil. Green (leaves) and brown (stems) asterisks shown next to the bars for normal P treatment indicate significant differences between P treatments within each species and in each tissue (Tukey test, p < 0.05). Bars represent standard error (n = 5).
Figure 6. Micronutrient concentrations, copper (A), iron (B), zinc (C), manganese (D) and boron (E), in leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels in the soil. Green (leaves) and brown (stems) asterisks shown next to the bars for normal P treatment indicate significant differences between P treatments within each species and in each tissue (Tukey test, p < 0.05). Bars represent standard error (n = 5).
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Figure 7. Macronutrient-to-phosphorus ratios, N/P (A), K/P (B), Ca/P (C), Mg/P (D) and S/P (E), in leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels in the soil. Green (leaves) and brown (stems) asterisks shown next to the bars for normal P treatment indicate significant differences between P treatments within each species and in each tissue (Tukey test, p < 0.05). Bars represent standard error (n = 5).
Figure 7. Macronutrient-to-phosphorus ratios, N/P (A), K/P (B), Ca/P (C), Mg/P (D) and S/P (E), in leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels in the soil. Green (leaves) and brown (stems) asterisks shown next to the bars for normal P treatment indicate significant differences between P treatments within each species and in each tissue (Tukey test, p < 0.05). Bars represent standard error (n = 5).
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Figure 8. Micronutrient-to-phosphorus ratios, Cu/P (A), Fe/P (B), Mn/P (C), B/P (D) and Zn/P (E), in leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels. Green (leaves) and brown (stems) asterisks shown next to the bars for the normal P treatment, indicate significant difference between P treatments within each species and in each tissue (Tukey test, p < 0.05). Bars represent standard error (n = 5).
Figure 8. Micronutrient-to-phosphorus ratios, Cu/P (A), Fe/P (B), Mn/P (C), B/P (D) and Zn/P (E), in leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels. Green (leaves) and brown (stems) asterisks shown next to the bars for the normal P treatment, indicate significant difference between P treatments within each species and in each tissue (Tukey test, p < 0.05). Bars represent standard error (n = 5).
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Figure 9. N/K (A), K/Ca (B), K/Mg (C), and Fe/Mn (D) ratios in leaves and stems of Eucalyptus and Corymbia species grown at normal and high P levels. Green (leaves) and brown (stems) asterisks, shown next to the bars for the normal P treatment, indicate significant difference between P treatments for each species and in each tissue (Tukey test p < 0.05). Bars represent standard error (n = 5).
Figure 9. N/K (A), K/Ca (B), K/Mg (C), and Fe/Mn (D) ratios in leaves and stems of Eucalyptus and Corymbia species grown at normal and high P levels. Green (leaves) and brown (stems) asterisks, shown next to the bars for the normal P treatment, indicate significant difference between P treatments for each species and in each tissue (Tukey test p < 0.05). Bars represent standard error (n = 5).
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Figure 10. Principal component analysis. Score (A) and loading (B) plots for PC1 vs. PC2 for nutrient ratios in the leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels in the soil.
Figure 10. Principal component analysis. Score (A) and loading (B) plots for PC1 vs. PC2 for nutrient ratios in the leaves and stems of Eucalyptus and Corymbia species grown under normal and high P levels in the soil.
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Table 1. Chemical analysis of the soil used in the experiment after nutritional correction with P to reach adequate (normal P) and high P (high P) levels.
Table 1. Chemical analysis of the soil used in the experiment after nutritional correction with P to reach adequate (normal P) and high P (high P) levels.
SoilOMpH CaCl2PresKCaMgH + AlCECBSSFeMnCuZnBPTotal
g/dm3 mg dm−3mmolc dm−3%mg dm−3mg kg−1
Normal P3.75.37.72.714.09.311.037.768.932.72.01.40.23.70.2152.3
High P3.75.445.36.112.79.312.040.969.936.72.71.50.22.80.2198.7
OM: organic matter; CEC: cation exchange capacity; BS: base saturation.
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Mazzafera, P.; Bulgarelli, R.G.; de Oliveira Silva, F.M.; de Andrade, S.A.L. Nutrient Ratios in the Leaves and Stems of Eucalyptus and Corymbia Species Under High Soil Phosphate. Forests 2025, 16, 869. https://doi.org/10.3390/f16060869

AMA Style

Mazzafera P, Bulgarelli RG, de Oliveira Silva FM, de Andrade SAL. Nutrient Ratios in the Leaves and Stems of Eucalyptus and Corymbia Species Under High Soil Phosphate. Forests. 2025; 16(6):869. https://doi.org/10.3390/f16060869

Chicago/Turabian Style

Mazzafera, Paulo, Rafaela Gageti Bulgarelli, Franklin Magnum de Oliveira Silva, and Sara Adrián López de Andrade. 2025. "Nutrient Ratios in the Leaves and Stems of Eucalyptus and Corymbia Species Under High Soil Phosphate" Forests 16, no. 6: 869. https://doi.org/10.3390/f16060869

APA Style

Mazzafera, P., Bulgarelli, R. G., de Oliveira Silva, F. M., & de Andrade, S. A. L. (2025). Nutrient Ratios in the Leaves and Stems of Eucalyptus and Corymbia Species Under High Soil Phosphate. Forests, 16(6), 869. https://doi.org/10.3390/f16060869

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