Evaluation of Gigantochloa scortechinii and soil interaction in three study sites in Malaysia

Abstract

Understanding the productivity and physiological status of an organ (rhizome) function can lead into a sustainable production of sympodial bamboo. Nutrient elements and ash content (AC) are among the indicators to indicate the productivity and physiological status of an individual bamboo organ. The present study aimed to (a) determine the concentration of macronutrient elements of Gigantochloa scortechinii's rhizomes at four different ages collected at three study sites, and (b) investigate their relationship with AC. The destructive sampling was conducted on a set of four consecutive rhizomes using the selective random sampling method. Middle rhizome wall portion was used to determine the macronutrient elements and AC. All primary and secondary macronutrients were found to be different (p ≤ 0.01) at different study sites, except for the magnesium (Mg). The changes in nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), and Mg from new sprout to mature rhizome showed a strongly positive relationship with AC. Thus, the N, P, K, Ca, and Mg concentrations decreased with rhizome age, resulting in a decrease in AC. The present study suggests that the suitable harvesting of individual bamboo culm and rhizome is at mature and older age while the remaining younger age bamboo is kept being grown so that the bamboo production is sustainable in terms of the physiological functions.

Gigantochloa scortechinii; Harvesting; Organ function; Physiological status; Sympodial.

1. Introduction

Bamboo is an evergreen plant; belonging to the grass family Poaceae (formerly Gramineae) and subfamily Bambusoideae [1]. Bamboo is a promising renewable material that can be seen in tropical and sub-tropical regions in Southeast Asia [2]. This plant with multiple usages possesses an important role in the socio-economic development in different countries because it is closely linked with humankind since the dawn of civilization [3]. In past few decades, the area of bamboo forests has significantly increased due to the high economic value of this plant, such as producing charcoal, furniture and young edible shoots, and its application in construction [4]. The global map of bamboo distribution indicates that this plant can grow in most countries, except European countries and Antarctica region, and is a native plant to Asia, Africa, Oceania and the Americas, predominantly in South and Southeast Asia [5].

Deliberating on the concept of ‘native invaders’ and the effects of native plants on their home ecosystem showed that available nutrients of the host habitats have been declining upon the expansion of the plants [6]. These super-dominant plant species, like bamboo, may impact the nutrient cycling, seed dispersion, pollination, as well as composition, function, and structure of their resident community. This long-term irreversible adjustment may convert the host ecosystem and cause micro-climatic modifications [7]. Some ecological characteristics of bamboo species, such as root exudation, litter quality, net primary production, stand density, and plant morphology have significantly impacted the soil ecosystem by altering the dynamics of food web, nutrients, carbon (C), nitrogen (N), Potassium (K), as well as changing the physical traits of the soil [8, 9]. Additionally, it has been shown that the invasion of bamboo may affect the rate of soil respiration, consequently causing a net increase in CO₂ emissions to the atmosphere as the ecosystem C stocks decline [10].

Bamboos are extremely competitive and adaptable, making them a suitable candidate for invading fragile ecosystems [11]. Reportedly, both clumping and running bamboos can be invasive; however, the rhizomatous clonal growth of running species is the important feature that promotes the invasion of bamboo [6]. Unlike woody plant species [12, 13, 14, 15] and other lignocellulosic plant materials, such as Hibiscus cannabinus [16, 17], the age-related changes during the maturations of individual bamboo culm or rhizome are the utmost imperative phase for research [18]. However, different bamboo organs possess different physiological functions that contribute to high growth performance and sustainable stand production. The growth performance and number of bamboo sprouts produce solely depend on the stimulation of rhizome buds and the sources of energy from their consecutive (older) rhizomes. The new sprout also has neither photosynthetic leaves nor rooting system to ensure its rapid elongation [19, 20].

With the exception of major chemical attributes, the amounts of all major chemical attributes—cellulose, lignin and extractives (alcohol and water soluble)—increase either slightly or significantly during the maturation period of an individual bamboo culm. In contrast, AC decreases as culms' age increases. The range of AC in bamboo varies from 1.10–4.70% depending on the organ, species, and position in culms [21, 22, 23, 24]. However, the present study focused on the rhizome (organ) of Gigantochloa scortechinii bamboo species. Our prior study found that all major chemical attributes, such as cellulose, lignin and extractives increased from new sprout to mature G. scortechinii's bamboo rhizome. But, the ash content (AC) decreased as the rhizome's age increased, and it also could not be used as a determinant factor for the decreasing of hydraulic conductance with rhizome age [25]. The ash refers to the inorganic residue left after incinerations at high temperature of a sample [26]; it is generally referred to as inorganic substances [21] and is a known indicator for determining the amount of inorganic nutrient elements in lignocellulosic materials [27]. Higher AC in raw material however could lead to undesired processing effectiveness and adversely affect the equipment used [28, 29, 30]. Additionally, understanding the changes in the nutrient elements of bamboo rhizomes with age, and their relationship with AC could improve the management and upstream activities of bamboo such as the culms selection for harvesting, fertilization and the expectation for future number of bamboo shoots; to achieve a sustainable organ function. Moreover, selecting culm or rhizome age for a lower AC material is useful for the downstream activities such as to avoid the dullness rate of machinery blade. Therefore, the present study aimed to determine the changes in macronutrient elements in the soil and plants, and their relationships with AC to gauge the extent that the decrease in the nutrients during the maturation of the G. scortechinii's bamboo rhizome was related to AC.

2. Materials and Methods

2.1. Geographical distribution of each study site

The soil and G. scortechinii Kurz ex Munro bamboo rhizome were sampled at three different locations in Peninsular Malaysia: Amanjaya Forest Reserve, Perak, Malaysia (5°37′12.46″N, 101°38′51.09″E); Kenaboi Forest Reserve, Negeri Sembilan, Malaysia (3°10′50.93″N, 101°58′37.60″E); and Ayer Hitam Forest Reserve, Selangor, Malaysia (3°0′16.17″N, 101°38′36.08″E) (Figure 1). These three forests were selected due to the abundance of G. scortechinii in the forests, and they represented the different peculiar site conditions such as elevation, disturbance, precipitation, temperature as well as relative humidity and soil conditions [31, 32].

Figure 1.

Map of three study sites: Amanjaya Forest Reserve, Perak, Malaysia (5°37′12.46″N, 101°38′51.09″E); Kenaboi Forest Reserve, Negeri Sembilan, Malaysia (3°10′50.93″N, 101°58′37.60″E); and Ayer Hitam Forest Reserve, Selangor, Malaysia (3°0′16.17″N, 101°38′36.08″E).

2.2. Climate condition of each study site

The data on climatic conditions (i.e. precipitation, number of rain days, temperature and relative humidity) of the four consecutive years were bought from the Malaysian Meteorological Department (Figure 2A and B).

Figure 2.

A. Mean annual number of rain days and precipitation at three study sites (Blue bar: Kenaboi FR; Red bar: Amanjaya FR; Purple bar: Ayer Hitam FR; Green line: Mean annual precipitation). B. Mean annual number of relative humidity and temperature at three study sites (Blue bar: Kenaboi FR; Red bar: Amanjaya FR; Purple bar: Ayer Hitam FR; Gold line: Mean annual temperature).

2.3. Soil sampling of each study site

Three soil sampling points about 1 m distance from the periphery of each G. scortechinii bamboo clump were set for soil sampling to avoid the effects of plant's variety on soil (Figure 3). The soil samples were collected at three depths of 0–20 cm, 20–40 cm and 40–60 cm to represent the zonation of G. scortechinii bamboo rooting zones and to further categorize the physical and chemical properties. A total of 81 soil samples were collected from all three depths around nine bamboo clumps in three study sites. All nine sub-samples (each depth) were composited to obtain one composited sample from each study site as it represented a field with similar vegetative history [33]. The composited samples were air-dried, ground and homogenized before sieving through a 2-mm mesh sieve and being stored within a sealed plastic container for further analysis.

Figure 3.

Three soil sampling points about 1 m from the peripheral of bamboo clump.

2.4. Physical properties of soil

The soil physical properties encompassed the soil bulk density, soil porosity and soil moisture content. The soil moisture content (MCO) was tested using the oven-dry value by quantifying the mass lost by a 2-gram soil after it was oven-dried at 105 °C for 24 h (22). The soil bulk density, particle density, and texture were determined following the procedure described by Jones [34].

2.5. Chemical properties of soils

Soil chemical properties encompassed soil pH, cation exchange capacity (CEC), total carbon (C), nitrogen (N) and sulfur (S), and available (extractable) phosphorus (P), potassium (K), calcium (Ca) and magnesium (Mg). The soil pH was determined using distilled water suspension [34] with glass electrode pH meter, Jenway 3505 (Essex, England). Approximately 25.0 g of homogenized soil sample was used for the determination of CEC using double acid method described by Chapman [35]. Subsequently, the leachate was examined using the atomic absorption spectrophotometer (PerkinElmer 5100 PC, Massachusetts, USA) for the Ca, K and Mg; and using the inductively coupled plasma-optical emission (PerkinElmer Optima 8300, Massachusetts, USA) for the P. The total C, N and S were determined using LECO TruMac CNS Analyzer (Michigan, USA).

2.6. Plant material sampling for Ash content measurements

Destructive sampling was performed using the selective random sampling method on a set of four consecutive G. scortechinii bamboo rhizomes from healthy clumps. The four consecutive rhizomes denoted four different rhizome ages i.e. new sprout, young; premature; and mature rhizome [31, 32] (Figure 4). Thirty-six rhizomes were sampled encompassing of four rhizome ages, three bamboo clumps and three study sites.

Figure 4.

Diagram of (a) four consecutive Gigantochloa scortechinii rhizomes, and (b) transverse section of the rhizome as adopted from Mohamed et al. [31].

2.7. Laboratory analysis

The middle rhizome wall portion was used to analyze the total concentration of primary macronutrients (N, P, and K), secondary macronutrients (Ca, Mg, and S) and the AC. The total N and S were determined using LECO TruMac CNS Analyzer (Michigan, USA). The total Ca, Mg, P and K were digested using the aqua regia method (ISO, 1995) and the concentrations were determined by using atomic absorption spectrophotometer (PerkinElmer 5100 PC, Massachusetts, USA) for the determinations of Ca, K and Mg, and by using inductively coupled plasma-optical emission (PerkinElmer Optima 8300, Massachusetts, USA) for the remaining nutrient elements. The AC was analyzed according to the standard American Society for Testing and Materials (ASTM) E1755-95 (2001) [36].

2.8. Statistical analysis

The macronutrient elements and AC were compared between three study sites and four rhizome ages using the factorial analysis of variance (ANOVA). The relationship between the macronutrient elements and the different study sites, rhizome ages, and AC were analyzed following Bivariate (Pearson) Correlation using IBM SPSS Statistics software version 25.0 (Armonk, New York, USA); the interpretations were based on Ratner [37]. The scatter plot was performed to regress the non-linear relationship between macronutrient elements, rhizome age and AC by using MS Excel version 2016 (Redmond, Washington, USA).

3. Results

3.1. The physicochemical properties of soils

We performed the experiment in three different sites: Amanjaya Forest Reserve, Perak, Malaysia; Kenaboi Forest Reserve, Negeri Sembilan; and Ayer Hitam Forest Reserve, Selangor, Malaysia. Each specific site demonstrated its unique physico-chemical traits, which could be considered for the qualitative measurements.

3.1.1. Physical properties of soil in three specific sites

The ANOVA results in Table 1 indicated that the soils’ physical characteristics in terms of bulk densities, soil porosity, and soil moisture were significantly different (p ≤ 0.01) in each site, individually. The highest soil bulk density (g cm⁻³) in all sites was observed in 40–60 cm depth soil while the lowest bulk density observed in soil surface (0–20 cm depth soil). The highest percentage of both soil porosity and moisture content in all sites observed in soil surface layer (0–20 cm depth soil) and the lowest observed in 40–60 cm depth soil.

Table 1.

Soil physical properties of three study sites: Amanjaya Forest Reserve, Perak, Malaysia; Kenaboi Forest Reserve, Negeri Sembilan; and Ayer Hitam Forest Reserve, Selangor, Malaysia.

Study Site	Depth (cm)	Physical Properties
		Bulk density (g cm−3)	Porosity (%)	Moisture content (%)
Amanjaya FR	0–20	0.97 ± 0.17c	61.20 ± 5.84a	63.29 ± 7.21a
	20–40	1.22 ± 0.11b	25.81 ± 3.57b	54.15 ± 6.08b
	40–60	1.42 ± 0.35a	11.80 ± 2.19c	46.49 ± 6.82c
Kenaboi FR	0–20	1.09 ± 0.08c	45.73 ± 5.02a	58.84 ± 4.37a
	20–40	1.38 ± 0.51b	21.14 ± 5.33b	48.07 ± 5.18b
	40–60	1.47 ± 0.70a	12.30 ± 4.15c	44.60 ± 5.73c
Ayer Hitam FR	0–20	1.10 ± 0.26c	46.01 ± 6.83a	58.48 ± 8.21a
	20–40	1.48 ± 0.75b	20.74 ± 3.76b	44.02 ± 6.14b
	40–60	1.51 ± 0.65a	16.62 ± 3.07c	43.14 ± 4.23c

3.1.2. The chemical properties of soil in three specific sites

The results of ANOVA analysis showed significant differences (p ≤ 0.01) in various soil chemical characteristics including pH, cation exchange capacity (CEC), total carbon (C), nitrogen (N) and sulfur (S), and available (extractable) phosphorus (P), potassium (K), calcium (Ca) and magnesium (Mg) inside each unique site, individually. In all sites, the highest soil pH observed in 40–60 cm depth soil while the highest CEC observed in 0–20 cm depth soil. The highest total (%) C, N and S in all sites observed in 0–20 cm depth soil. The 0–20 cm depth soil also contain highest extractable (μg g⁻¹) K and Mg (Table 2).

Table 2.

Soil chemical properties of three study sites: Amanjaya Forest Reserve, Perak, Malaysia; Kenaboi Forest Reserve, Negeri Sembilan; and Ayer Hitam Forest Reserve, Selangor, Malaysia.

Study site	Depth (cm)			Chemical properties
		pH	CEC (cmol kg−1)	Total (%)			Extractable (μg g−1)
				C	N	S	P	K	Ca	Mg
Amanjaya FR	0–20	4.49 ± 0.1b	13.29 ± 1.4a	3.12 ± 0.0a	0.30 ± 0.0a	0.04 ± 0.0a	65.10 ± 2.13c	125.90 ± 7.98a	470.10 ± 8.86a	170.10 ± 9.30a
	20–40	3.89 ± 0.0c	9.71 ± 0.8b	2.03 ± 0.0b	0.16 ± 0.0b	0.02 ± 0.00b	128.80 ± 5.87a	33.60 ± 8.14c	233.50 ± 9.73c	28.20 ± 5.66c
	40–60	4.85 ± 0.3a	3.99 ± 0.7c	0.99 ± 0.04c	0.11 ± 0.07c	0.01 ± 0.00c	86.80 ± 9.04b	56.92 ± 6.55b	256.70 ± 5.84b	51.30 ± 5.71b
Kenaboi FR	0–20	4.6 ± 0.10c	15.86 ± 2.57a	1.55 ± 0.12a	0.15 ± 0.03a	0.03 ± 0.00a	67.55 ± 5.92a	98.55 ± 3.27a	302.90 ± 9.98a	87.00 ± 8.65a
	20–40	4.19 ± 0.2b	8.21 ± 1.32b	0.74 ± 0.0b	0.08 ± 0.01c	0.01 ± 0.01b	57.12 ± 5.03c	22.00 ± 8.14c	257.60 ± 7.56c	26.40 ± 3.18c
	40–60	5.03 ± 0.57a	4.56 ± 0.96c	0.65 ± 0.07c	0.08 ± 0.0b	0.01 ± 0.00c	65.94 ± 7.68b	43.76 ± 3.20b	260.70 ± 5.81b	30.20 ± 3.77b
Ayer Hitam FR	0–20	4.68 ± 0.3b	15.43 ± 2.5a	1.25 ± 0.03a	0.12 ± 0.05a	0.03 ± 0.0a	96.60 ± 5.31a	76.83 ± 7.52a	274.10 ± 9.87b	59.70 ± 6.89a
	20–40	4.23 ± 0.6c	9.21 ± 1.08b	0.56 ± 0.0b	0.06 ± 0.01c	0.01 ± 0.0c	65.80 ± 6.88c	22.90 ± 2.83c	292.10 ± 4.29a	23.20 ± 4.56c
	40–60	4.98 ± 0.8a	5.05 ± 0.79c	0.52 ± 0.05c	0.07 ± 0.0b	0.02 ± 0.0b	84.70 ± 6.79b	39.84 ± 2.37b	247.10 ± 4.05c	28.80 ± 4.38b

Note: FR = Forest Reserve; CEC = cation exchange capacity; C = carbon; N = nitrogen; S = sulfur; P = phosphorus; K = potassium; Ca = calcium; Mg = magnesium; ± = standard error.

3.2. The macronutrient Elements and ash content of plants Harvested from three sites

This experiment was divided into two main steps as follows: I) in the first step, we tested macronutrient and ash contents of plants harvested from each specific site; II) in the second step, we evaluated the macronutrients and ash contents of four different rhizome ages, which are new sprout, young rhizome, pre-mature rhizome, and mature rhizome.

3.2.1. Analysis of macronutrients and ash contents of bamboo in each site

The macronutrient elements encompass primary macronutrients (N, P and K) and secondary macronutrients (Ca, Mg and S). The ANOVA test results indicated that all measured macronutrients and the AC were significantly different (p ≤ 0.01) within the study site except Mg (Figure 5). The highest amount of N, P, K, Ca, Mg, S, and ash content were observed in the plants which were harvested from Amanjaya Forest Reserve with 10.13, 6.34, 9.68, 3.12, 3.44, 0.28, and 25.36 mg g⁻¹, respectively (Figure 5). On the other, the lowest N, P, K, and Ca were reported in the bamboos harvested from Ayer Hitam Forest Reserve with 9.31, 5.88, 7.83, and 2.54 mg g⁻¹, respectively (Figure 5). Furthermore, the lowest amount of M, S, and ash content were in the bamboos of Kenaboi Forest Reserve with 3.4, 0.21, 20.3 mg g⁻¹, respectively (Figure 5).

Figure 5.

The Duncan's multiple range tests for the effects of study site on the macronutrient elements and ash content.

3.2.2. Evaluation of the macronutrients and Ash contents of four different rhizome Ages

The ANOVA results analysis showed that there were significant differences (p ≤ 0.01) between the measured macronutrients and the AC contents in all four different rhizome ages. However, the ANOVA results also showed a significant difference (p ≥ 0.05) only for the S content of four different rhizome ages (Figure 6). The Duncan's multiple range tests showed the highest amount of N, P, K, Ca, Mg, S, and ash content in the new sprout of bamboo with 12.28, 6.96, 13.42, 4.01, 4.87, 2.67, and 31.43 mg g ⁻¹, respectively (Figure 6). In contrast, the lowest amount of N, P, K, Ca, Mg, S, and ash content were reported in mature rhizome with 8.08, 5.46, 6.53, 2.2, 2.58, 0.27, and 18.88 mg g⁻¹, respectively (Figure 6).

Figure 6.

The Duncan's multiple range tests for the effects of rhizome age on the macronutrient elements and ash content.

The results of Pearson's correlation coefficient test between macronutrient elements, rhizome age, and ash content showed the high positive correlation between N with P, K, Ca, and AC content with 0.869, 0.885, 0.874, and 0.827, respectively. However, a high negative correlation was reported between N and age of rhizome with -0.912 (Table 3). The high positive correlations were also observed between P and K, Ca, Mg, and AC with 0.891, 0.914, 0.823, and 0.928, respectively. Similarly, a high negative correlation was observed between P and rhizome age with -0.834 (Table 3). High positive correlations were reported between K and Ca, Mg, and AC with 0.946, 0.826, and 0.871, respectively. In contrast, a high negative correlation was observed between K and rhizome age with -0.844 (Table 3). Ca showed a high positive correlation with Mg (0.865) and AC (0.903) whereas a high negative correlation was reported between Ca and rhizome age with -0.834 (Table 3). Although the high positive correlation was observed between Mg and AC with 0.836, the high negative correlation was also reported between Mg and rhizome age with -0.899 (Table 3). There is no significant correlation between S and rhizome age as well as AC (0.000 and 0.235, respectively) (Table 3). Finally, a high negative correlation was also seen between rhizome age and AC with -0.823 (Table 3).

Table 3.

The Pearson's correlation coefficient between macronutrient elements, rhizome age, and ash content.

Element	N	P	K	Ca	Mg	S	Age	AC
N	1	0.869∗∗	0.885∗∗	0.874∗∗	0.913∗∗	0.016ns	−0.912∗∗	0.827∗∗
P		1	0.891∗∗	0.914∗∗	0.823∗∗	0.118ns	−0.834∗∗	0.928∗∗
K			1	0.946∗∗	0.826∗∗	−0.012ns	−0.844∗∗	0.871∗∗
Ca				1	0.865∗∗	0.065ns	−0.834∗∗	0.903∗∗
Mg					1	0.125ns	−0.899∗∗	0.836∗∗
S						1	0.000ns	0.235ns
Age							1	−0.823∗∗
AC								1

Note: ns = not significant at p < 0.05, ∗ = significant at p < 0.05, and ∗∗ = highly significant at p < 0.01.

The result of regression test confirmed the strong coefficient of determination value (R² = 0.880) of N when the age of rhizome was increased. Furthermore, K decreased (R² = 0.865) dramatically from new sprouts to young rhizomes, and then gradually decreased to mature rhizomes. In addition, Ca dramatically decreased (R² = 0.859) from new sprouts to young rhizomes, before gradually decreasing to mature rhizomes. On the other hand, a non-linear regression (R² = 0.886) was reported when Mg decreased dramatically from new sprouts to pre-mature rhizomes and remained constant in mature rhizomes (Figure 7).

Figure 7.

Relationship of macronutrient elements with four rhizome ages (1: New sprout; 2: Young; 3: Per-mature; 4: Mature).

There were strong linear relationships between N (r = 0.827), P (r = 0.928), K (r = 0.871), Ca (r = 0.903) and Mg (r = 0.836) and AC; however, that was not observed between S (r = 0.235) and AC (Table 3). Thus, the AC concentrations increased with increasing N, P, K, Ca, and Mg. The results in Figure 8 further demonstrates those relationships using non-linear regressions of N, P, K, Ca, and Mg with AC (R² = 0.702, 0.862, 0.797, 0.818, 0.715, respectively) (Figure 8).

Figure 8.

Relationship between macronutrient elements and ash content.

4. Discussion

Soil is a part of the terrestrial environment and supports a great amount of life forms. Soil health represents the continuous capacity of soil to function as a living ecosystem, depending highly on the different ecological processes governed by soil organism. The analytical results of chemical properties are presented in Table 1. In all sites, all chemical properties were higher in surface than subsurface soils, except for P and Mg. The content of C, N, and S slightly decreased. Meanwhile, K (Kenaboi FR and Ayer Hitam FR only), Ca, and Mg (Mg for Kenaboi FR only) showed a large decrease as the soil depth increased. The chemical contents from 0-20 cm to 20–40 cm significantly decreased by almost half of the chemical composition. Meanwhile, the chemical compositions from 20-40 cm to 40–60 cm were only slightly different. Enhanced chemical properties accumulation in the topsoil is attributed to the continuous input of organic matter from plant and animal residues as well as root exudates that increase the mineralization and accumulation of organic matter. Likewise, Liu et al. [38], Tufa et al. [39] and Weldmichael et al. [40] found that the soil organic matter (SOM) greatly decreased with increasing of soil depth.

Comparing the composition between chemical content, Ca showed the highest chemical composition among all chemical contents, and Amanjaya FR had the highest Ca compared to Kenaboi FR and Ayer Hitam FR. Different composition of chemical properties in different site might be affected by different forest types or forest functions, and forest disturbance level. Mohamed et al. [31, 32] stated that Amanjaya FR had natural stand conditions at elevation of 700 m above sea leval and the area was an active forest production area and wildlife (elephant) habitat. The low disturbance level and its role as wildlife habitat at high elevation resulted in natural and slower decomposition process compared to forest with high disturbance level at low elevation. For example, Kenaboi FR was a natural stand at elevation 320m and highly disturbed as a recreational site while Ayer Hitam FR was a planted forest at elevation 300m with medium disturbance as an education and research area. Likewise, all chemical properties were found higher in Amanjaya FR compared to the other sites (Kenaboi FR and Ayer Hitam FR).

4.1. Nitrogen concentration

A significant difference in total N was found at all three soil depths in all three study sites (Figure 5). Although some genes have been reported to be involved in N (in form of nitrate) uptake and mediated long-distance translocation; the ability to translocate N is generally limited by the availability of N concentration in the root (source organ), and the N uptake ability solely depended on the available N concentration in soil solutes. Furthermore, the difference of available N in soil solute is influenced by several factors [41, 42]. Significant differences between factors such as precipitation, temperature, soil properties and other environmental factors among study sites can be observed in Table 1 and Figure 5. Therefore, the difference in the available N in soil solutes at different sites could be the main reason to the difference in N (p ≤ 0.01) in the rhizome samples.

Regarding rhizome age, the new sprouts had the highest N (12.30 mg g⁻¹), followed by young (10.6 mg g⁻¹), pre-mature (8.20 mg g⁻¹) and mature rhizomes (8.10 mg g⁻¹) (Figure 6). A strong negative (r = −0.912) relationship (Table 2) and higher coefficient of determination value (R² = 0.880) (Figure 7) illustrated that the N markedly decreased from new sprouts to mature rhizomes. This is consistent with prior study on Phyllostachys pubescens [43].

The lower average N in rhizomes (Figure 6) is also possibly related to the development phase of new sprouts where they absorb a large amount (∼40.5%) of N as they grow [44]. The higher amount of N required for the growth of new sprouts also suggests the remobilization of N from senescing organs such as leaves, culms, and rhizomes at the vegetative stage [45, 46, 47].

Furthermore, some uptaken N assimilate into the root while a larger portion is transported to the shoot through biochemical pathway [47]. The assimilation and transportation depend on the availability of carbon skeletons to assimilate N into amino acids [48], and on the supply of adenosine triphosphate [49], ferredoxin and nitrate reductase [50] as products of photosynthesis, respiration, and photorespiration pathways. Therefore, these attributes lower the N concentration of premature and mature rhizomes, depicting the presence of their active photosynthetic leaves.

4.2. Phosphorus concentration

The difference of extractable P in soil (Figure 5) could be related with the difference (p ≤ 0.01) of P in rhizome among study sites (Figure 7). The potential duration of P used during the early growing phase as facilitated from remobilization is dependent on the available P stored and P requirement for current growth; however, it is unlikely to last longer than a few weeks [51, 52]. Later, the growth is mostly dependent on P uptake from the soil solute [51].

The deficiency of available P causes reduction in the growth such as height and diameter and decrease in export of cytokinin from roots to growing organ before the internal or stored P decreases [53, 54]. Inversely, under sufficiently available P, the P concentration in plant and the growth are not deterred by P uptake and P stored in organ. However, it is affected by other factors such as light intensity, temperature, P losses from storage organs [55] and incorporated cation-anion balance (P, K and N) in xylem, reflecting the availability of another nutrient in soil solute [56].

The rhizome age explained up to 78.09% of the variation in P (Figure 6). The decreasing trend of P with age agrees with previous studies on P. pubescens [43, 57]. It could be related to a high P use efficiency [53] in bamboo. The youngest rhizome and growing organ have the greatest import of P both from the root uptake and remobilization from the senescent organ [51, 52]. The increasing P concentration in growing organs is evidently synchronized with the decreases of P concentration in senescing organs. After the full expansion and in the late vegetative phase, the decreasing growth rate reflects lower light condition of older leaves due to self-shading, increase in respiration, and beginning of senescence of older organ [50], such as leaves, branches, and rhizomes in individual culms.

The decrease of growth occurs even under sufficiently available P conditions. At this stage, P uptake by roots (uptake-dominated P supply) decreases and by far, the most important P source is from the remobilization of P from senescing organs (remobilization-dominated P supply). The P remobilization efficiency can reach up to 90% of the initial P stored in a senescence organ before death, which is incorporated into a growing organ by proportionate mobilization and appropriate remobilization (recycle) to the source organ to maintain cell function [56]. The P remobilization efficiency during late vegetative could also be associated with the present of new shoot leaves and nodal roots at culm nodes of mature and over-mature bamboo culms as anecdotally observed during sampling.

4.3. Potassium concentration

The significant difference (p ≤ 0.01) of K among study sites (Figure 5) could be related with the concentration of extractable K in soil's rooting zones (Figure 5). Similar with N and P, the requirement of K during early vegetative growth is mostly facilitated by the remobilization of K stored in the source organ and the senescence of one before it is significantly facilitated through K uptake from the soil solute [52]. This depicts that K in plant or organ relies on the ability of the roots to obtain K from the mobilization and roots uptake from the soil solute which are synchronous with the K use efficiency [58]. The environmental factors (Table 1), such as available nutrients (Figure 6) and nutrient-nutrient interaction in soil solute has a major role in the availability of K in soil solute. This significantly influences the K uptake and K use efficiency [58, 59]. The requirement and the uptake of K are also directly related to N to meet the requirement for optimal growth [58, 60].

The result corroborated Umemura and Takenaka [57]. Wu et al. On the other hand, suggested that the decreasing nutrient concentrations such as N, P and K from new sprouts to mature P. pubescens culms were due to a dilution effect resulting from quick increases in biomass. These show that the older culms contain less N, P and K, and more cellulose as they grow. The differences in K with rhizome age is also suggested to be related with growth, photosynthesis rates, K supply from root uptake from the soil solute, and the physiological adaptation of K [58, 59].

The high K concentration (13.42 mg g⁻¹) in the new sprout rhizome samples (Figure 6) could be due to high import of K from remobilization of reserved K and from the root uptake to furnish higher K requirement for fast growth [52, 58]. The requirement of K during rapid vegetative growth exceeds the concentration of K supply and the remobilization could therefore take place from active photosynthetic leaves [61]. The new sprout of bamboo grows with neither root nor photosynthetic leaves (anecdotal evidence); thus, the K supply is fully employed from the root uptake and remobilization from subsequent older culms and rhizomes. Therefore, both the photosynthesis rates and physiological adaptation of K could imply the decreasing of belowground (rhizome) K in the present study (Figure 7) [62, 63].

4.4. Calcium concentration

The significant difference (p ≤ 0.01) in Ca at different study site (Figure 5) could be due to the difference of Ca concentration in soil solutes at different study sites (Figure 5). This is because, Ca has a low ability for re-remobilization; therefore, it is not only restricted in the metaxylem, but also contributing in the cell wall of adjacent cells [64]. It is involved in cell structural development of growing organs, and its translocation to growing organs is observed from root uptake rather than from mature leaves [57]. The difference could have appeared due to the limitation of uptake and accumulation when other cations such as Mg is higher in soil solutes [65].

The results agree with a study by Umemura and Takenaka [57]. However, Wu et al. [43] identified an alternate-years trend in P. pubescens culms that could be related to a strong biennial variation of new bamboo shoots production in a monopodial bamboo species and be influenced by intrinsic leaf age structure [44].

4.5. Magnesium concentration

Although Mg uptake and concentration in plant could be either exhibited or inhibited by the interaction of nutrient elements in soil solute [65, 66], the discriminatory mechanisms for uptake, transport, accumulation, and remobilization of Mg [67] could be one of the factors for the insignificant Mg among study sites (Figure 5). This can be considered because all three study sites are under natural disturbance of forest conditions (no treated nor fertilized). The difference in soil pH (Table 1) is also influenced by the Mg uptake rather than other cations (such as K, Ca, and Na) in soil solute [68].

Moreover, the deficiency of Mg uptake due to the antagonist effect of nutrient-nutrient elements (such as limited Mg uptake by excessive K in soil solute) is noticeable on leaves rather than root Mg concentration [65]. Magnesium deficiency also affects the quality of plant morphological characteristics, induces physiological changes, alters plant signaling, retards growth and accelerates aging processes [66]. These show the physiological function of Mg for photosynthesis and as a cofactor with ATP in enzymatic reaction [69] including the role of Mg in phytochemical attributes [66]. Therefore, the insignificant Mg concentration of rhizomes among study sites is also suggested to have a pronounced effect on the morphological characteristics and growth performance before the symptoms are observable in the stored organs (rhizome).

The result, however, was found to contradict with a study on P. pubescens culms by Wu et al. [43]. Magnesium is a phloem-mobile nutrient element [67] and several Mg transporter genes such as AtMGT1, AtMGT5 and AtCNGC10 have a major role in Mg uptake, translocation, remobilization, and long-distance transport [66, 71, 72].

The remobilization of Mg from the source organ to the new sprout could imply the higher Mg concentration of the new sprout (Figure 6). The Mg from the older age rhizome (young, pre-mature and mature rhizome) is also transported to active photosynthetic leaves to mediate cation-anion balance and to maintain cell turgor [73], and up to 75% of leaves Mg are involved in protein synthesis [70]. Similar with N, P and K, the decreasing trend of Mg concentration in rhizome across the rhizome ages is expected to pronounce with both the remobilization of Mg to meet the new sprout requirement and to support the requirement of active photosynthetic leaves.

4.6. Sulfur concentration

The S concentration in rhizomes had a relatively low range, 0.20–0.40 mg g⁻¹. Although the variations of S concentrations are relatively small, statistically they were different (p ≤ 0.01) across the study sites (Figure 5). The nutrient-nutrient interactions could be a limitation of S (as well as N and P) absorption [55]. The available S (inorganic form) for plant uptake generally accounts for less than 10% in soil solute [73, 74, 75, 76], illustrating the important roles of the mineralization of organic S into inorganic S [77].

The mineralization process of organic S in soil solute involves either biological or biochemical process [78]. However, the process in the forest area is low if compared to agricultural area due to the forest litter quality in forest area [79]. The organic S present in solute is in a steady state, but rapidly changes from one organic S form to another by microbial process [77]. Under limited nutrient supply, the S uptake is not significantly influenced by growth, but only by the limited available nutrients in soil solute [80, 81]. Thus, this may imply the difference in S in rhizome samples among study sites in the present study.

There is no difference in S concentration with rhizome age and the interaction of study site and rhizome age (Figure 5, Figure 6). The S translocated into xylem is mostly in the form of sulphate ion, which exhibits a higher translocation rate in the metaxylem to the growing organs [82], such as the apex of new sprout and new leaves in bamboo. The translocation into new leaves depicts that a large portion of total S uptake is assimilated into cystine, cysteine and methionine for the formation of chlorophyll while a small portion retains in the source organ. Therefore, although the reduction of S can take place in the source organ, it can be significant in leaves [79]. This could be one of the reasons for the insignificant changes of S in different rhizome ages.

Furthermore, the S stored in rhizomes can be retrieved via the translocation pathway by sulphate transporter-2 and sulphate transporter-3, which have been shown to be the determinants of sulphate distribution factors among organs [83, 84]. Although this suggestion would satisfactorily explain the constant S concentration observed in the rhizomes sample, our study could not clarify this hypothesis, and thus further study is needed in the future to determine its accuracy.

4.7. Relationship of macronutrient elements with ash content

The decrease in AC is possibly related to the decreasing ability of the bamboo rhizomes to absorb nutrients from soil as they age. The growth performance, productivity hydraulic resistance in bamboo rhizomes is strongly related to the ontogenetically and physiologically age-related factors [32]. This correlates with the structural development and modification seen during maturation of individual bamboo rhizomes and breakdown in the conducting systems [24, 32, 85]. Furthermore, the decreases in AC during maturation are related to metabolically active vascular tissues translocating the nutrient elements; a process that is crucial for the fast growth of bamboo organs [43, 57]. The decreases in nutrient concentrations are also due to the dilution effects of quick increases in biomass [43] that increase the major chemical attributes, such as holocellulose, lignin and extractives during maturation of bamboo culms [24] and rhizomes [25].

5. Conclusions

The differences in N, P, K, Ca, and S concentrations with study sites were attributed by the availability of respected nutrients in soil solute and the peculiar site conditions which blend different environmental conditions. But the insignificance of Mg concentration of rhizome with study site is expected to cause a pronounced effect on the morphological characteristics and growth performance rather than the Mg concentration in rhizome. The decreasing N, P, K, Ca, and Mg concentrations in rhizome with rhizome age are expected to be impacted by both the remobilization of respected nutrients to meet the new sprout requirement and the morpho-physiological status of individual bamboo organs. The decrease in AC concentrations from new sprouts to mature rhizomes was related to the concentrations of the respected nutrient elements. Therefore, in terms of sustainable production, we recommend avoiding cutting less than mature bamboo, including both culm and rhizome due to its physiological functions.

Declarations

Author contribution statement

Conceived and designed the experiments - Johar Mohamed; Hazandy Abdul-Hamid ts.

Performed the experiments - Johar Mohamed; Eliza Mohamed; Fatin-Norliyana Mohamad-Ismail.

Analyzed and interpreted the data - Johar Mohamed; Abdul-Majid Jalil; Puteri-Edaryoyati Megat-Wahab.

Contributed reagents, materials, analysis tools or data - Mostafa Moradi; Hamid-Reza Naji.

Wrote the paper - Johar Mohamed; Rambod Abiri.

Funding statement

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Data availability statement

Data included in article/supp. material/referenced in article.

Declaration of interest's statement

The authors declare no competing interests.

Additional information

No additional information is available for this paper.