Introduction

The mangrove is a plant community that colonizes the muddy shores of sheltered estuaries (Ong et al. 1991). Mangrove biodiversity is almost five times higher in the Eastern Hemisphere than the Western Hemisphere and is composed of 58 species compared to 12, respectively (Duke 1992). More than 60 species of true or exclusive mangrove species have been recorded in the world. The Indonesia-Malaysia region contained the most species, with 48 (Duke et al., 1998). There are approximately 675,000 ha of mangrove forests in Malaysia, but only 11,000 ha could be found in Peninsular Malaysia (Soepadmo, 1998). Of the total forested land in Malaysia, 441,092 ha (70%) have been declared to be forest reserves, and there are currently approximately 112 mangrove forests in the country (Shahrul et al. 2006). Mangrove species possess common characteristics that enable them to tolerate a wide range of salinities, suggesting convergent adaptation between these species (Liang et al. 2008).

Soil chemical and physical properties of mangrove forest indicate the status of soil fertility level. Thus, information on soil property can be used for enhancement of soil quality and governing ideal ecosystem. As medium for mangrove trees growth, soil should be able to supply enough nutrient and have good characteristics to ensure better trees performance and established greater forest ecosystem for wildlife conservation, economic value, and most importantly, to balance environmental condition. Unfortunately, it is surprisingly this important factor in mangroves have received relatively little attention. Previous researchers have studied some soil factors in relation to the simpler communities (Clarke and Hannon 1967), but their study did not attempt to examine soil characteristics and their current nutrient status in plant roots. Therefore, it is very important to perform this study at the Matang mangrove forest because it is the best managed mangrove forest in the world, especially used for timber production. However, information on the link between mangrove soil characteristics and the nutrient status of the trees is still scant. Answers to these questions are urgently needed considering the increasing demand for the future conservation of mangroves. Therefore, the present investigation was designed as an attempt to determine the soil characteristics in a Matang mangrove area and to compare the nutrients status of mangrove trees (Rhizophora apiculata) between different age classes. Thus, the present study will increase the recognition of Malaysian mangrove forests as valuable resources for future generations, both in terms of their economic value and the ecosystem services they provide.

Materials and methods

Collection of Mangrove plant parts and soil samples

The study was conducted at the Matang Mangrove Forest Reserve (100° 36′N, 4° 50′E) (Fig. 1), which is located in Kampung Kuala Sepetang sub-locality, Kuala Sepetang locality in the state of Perak, Peninsular Malaysia, in a 40,800-ha area covered with mostly even-aged (1–30 years) stands of Rhizophora apiculate trees. Except for the Mount Babu and Maxwell Hill peaks, the mangrove forest area is almost entirely flat, a dominant feature of the coastline. In this locality, the land is almost entirely cultivated and settled, except for the coast. The climate is mainly equatorial, with a mean annual temperature of 23–30 °C. The average rainfall ranges from 2000 to 3000 mm. This area experiences semi-diurnal tides ranging from 1.6 to 2.9 m (Mohamad Pazi et al. 2021). Soil and root samples were collected from the productive areas in September 2012. These productive areas were divided into three categories as follows: the youngest category included 1- to 10-year-old trees, the immediate category was 11- to 20-year-old trees and the oldest categories were 21- to 30-year-old trees (Table 1). For better visibility and clarity reasons, the results presented and discussed in this study concern 5- and 10-year-old trees as the youngest category, 15 and 20-year-old trees as the immediate category, and 25-year-old trees as the oldest categories.

Fig. 1
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Map of Peninsular Malaysia showing the location of the Matang mangroves area (Putz and Chan 1986) with the insets showing the approximate location of the study area (source: Google Map 2014)

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Table 1 Properties of productive areas categories based on tree aged
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Five soil samples were taken at 0 to 15 cm depth using a peat auger (Eijkelkamp, Giesbeek, the Netherlands) in each category of the productive areas as mentioned above. The samples were air-dried and sieved to pass a 2 mm sieve size for further physical and chemical analyses. Five healthy Rhizophora apiculata trees were randomly selected from each category in productive areas. The age of the stand of trees was determined by a forest ranger based on their diameter at breast height (DBH) (Gong and Ong 1990). The living and healthy support roots that directly pierced the soil were collected from above and below ground. The root samples were carefully washed with clean water to loosen the muddy soil around each root. The fresh weights of all samples were recorded. The samples were oven-dried at 80 °C for 1 week to obtain their dry weight and then were ground into powders for further nutrient analyses. The present research will only focus on nutrient statuses, such as total carbon (C), total nitrogen (N), phosphorus (P), and silicon (Si).

Soil and plant tissue analyses

Soil analyses

Soil particle analyses: the sampling of the surface layer was performed at a depth of 0 to 15 cm. The soil samples were left overnight in Calgon solution, and the soil particle size was determined using a particle size analyzer (Malvern Mastersizer 2000, Malvern Panalytical Ltd; Malvern, UK). The US Department of Agriculture (USDA) texture triangle was used to determine the soil texture. Soil pH and soil electrical conductivity - soil pH (Hendershot et al. 1993) and soil electrical conductivity (Rhoades 1982) were measured using a ratio of 1:2.5 and 1:5, respectively by using a pH meter (Model Metrohm 827, Riverview, FL, USA) and electrical conductivity meter (METTLER TOLEDO SevenEasyTM Conductivity Meter S30, Hamilton, New Zealand). Carbon content - total carbon (C) in soil samples was analyzed using the TruMac CNS macro analyzer (LECO Corp., USA). Nitrogen content - total nitrogen (N) was determined using the Kjeldahl digestion procedure described by Bremner and Mulvaney (1982). Available P was determined using the Bray II method (Bray and Kurtz 1945). The N and P contents in the solution were determined using an Auto Analyser (AA) (Lachat QuikChem® 8500 Series 2 FIA System (FIA+), USA). Soil cation exchange capacity - the soil exchange capacity (CEC) was determined using the neutral ammonium acetate extraction method (Schollenberger and Somin 1945). The available Si in soil samples was extracted using sodium carbonate (Na2CO3) and ammonium nitrate (NH4NO3) (Korndӧrfer et al. 2004). The Si standard was prepared and its concentration in the solution was determined by the colorimetric molybdenum methods at 600 nm with a spectrophotometer (UV-1700 PharmaSpec, Shimadzu Instruments). The same procedure was followed by using 10 mL of sample solution to determine Si concentration. The nutrient concentrations, whether in mg kg−1 (ppm, parts per million) or percent (%) are always based on the weight of dry matter instead of the fresh weight. Fresh weight includes both the weight of the dry matter and the weight of the water in the tissue. Since the percentage of water can vary greatly, by convention, all concentrations of elements are based on dry matter weights.

Plant analyses

The roots samples were digested using a wet acid digestion protocol described by Jones et al. (1991). Briefly, concentrated sulfuric acid (H2SO4) and 50% hydrogen peroxide (H2O2) were used to digest the root tissues. An Auto Analyser (AA) (Lachat QuikChem® 8500 Series 2 FIA System (FIA+), USA) was used to determine the presence of N and P elements. The Si content in root samples was determined by the autoclave-induced digestion (AID) procedure (Moyer et al. 2008). The methods used a mixture of 2 mL of 50% hydrogen peroxide (H2O2) and 3 mL of 50% sodium hydroxide (NaOH) followed by autoclaving at 103 kPa (15 psi) for 30 min. In some cases of incomplete digestion, 2 mL of hydrogen peroxide was added, and the volume was increased to 50 mL with distilled water. The Si in solution was determined as mentioned for the soil.

Classical statistical analysis

The Statistical Analysis System 9.2 (SAS) was used to determine the basic statistical description by means of separation at 5% with an LSD test (SAS 2000).

Results

Soil physicochemical properties

The coefficients value (CV) for the soil pH, EC, and CEC were less than 10%, and the pH was identified as the lowest CV (Table 2). The mean pH value was found to be less variant in this study area. Most of the pH values recorded in this study were less than seven. The pH of the soils in this study area was consistently within the range of 6.22 to 6.97 at all sites (Table 2). The soil EC was between 7.77 and 8.58 dS m−1. The soil CEC ranged from 22.29 to 25.29 cmolc kg−1 soil. The physical properties of the soil in the mangrove sites showed very minor variations (Table 3). All the soil samples were composed of less than 35% sand particles at a soil depth of 0 to 15 cm. The particle size distributions were mainly dominated by silt (37.05–37.21%), with clay and sand contents of 30.06–31.08 and 29.05–30.09%, respectively (Table 3). The soil texture was clay loam.

Table 2 Summary statistic of soil chemical properties in Matang mangroves
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Table 3 Physical properties of the soil in the Matang mangrove forests
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Nutrient status of Matang mangrove roots and soil

Generally, the results of nutrient status among mangrove parts (roots and soils), productive area categories (youngest, immediate, and oldest), and tree aged (5, 10, 15, 20, and 25 years) showed an inconsistent pattern, which may have been influenced by the soil characteristics in the present study. In mangrove roots, there was an interaction (p ≤ 0.05) between productive area categories and tree age for the total N and P. The oldest tree roots had more N and P in root tissue compared to the youngest trees. The results observed in our study showed that N and P in the oldest productive area (25-years old trees) were higher than in immediate productive categories (15- and 20-year-old trees) followed by the youngest productive categories (5 and 10-years old trees). The total N content ranged from 0.24 ± 0.06 to 0.36 ± 0.06% in the roots (Table 4). The available P ranged from 0.06 ± 0.01 to 0.10 ± 0.02% in the roots (Table 4). This is attributed to the accumulation of plant nutrients with time, such as N and P during the growing period for the biomass formation of mangrove trees. Older trees had more roots and a greater chance of roots contact with soil solution for roots absorption.

Table 4 The nutrient content in the root samples of Mangrove collected in Matang area
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In mangrove soils, there was an interaction (p ≤ 0.05) between productive area categories and tree aged for the total C, total N, and available P (Table 5). Mangrove soils that have been collected in the youngest productive area categories (5 and 10-year-old trees) had the highest nutrient concentration compared to immediate productive area categories (15 and 20-year-old trees) and followed by the oldest productive area categories (25-year-old trees). The total C ranged from 15.21 to 15.93% in soils (Table 5). Since the total C as measured by this method was less than 22%, hence, the soil is classified under mangrove forests as a mineral. Our results showed that the total N was low, ranging between 0.57 and 0.66%, and the soil available P ranged between 25.70 to 33.07 mg/kg soil (Table 5). The highest C:N ratio proved that mangrove soils may approach N limitations. The high C:P ratios confirmed that there were P limitations in the soils when the concentration of available P was lower than the total organic C. This total C in the top 0–15 cm in the soil sample is mainly derived from the terrestrial environment, mainly from mangrove forest plant’s part and some organisms.

Table 5 Average nutrients and its ratios in Matang mangrove soils
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There was no interaction (p ≥ 0.05) between productive area categories (youngest, immediate, and oldest), tree aged (5, 10, 15, 20, and 25 years old) and available Si content (root and soil). However, there was significant different (p ≤ 0.005) between root and soil even though the amount of available Si in root was not markedly different than the available Si in the soil. The range of available Si in the soil was ranging between 111.16 ± 2.85 and 120.08 ± 4.04 ppm whereas; the amount of available Si in root was ranging from 113.60 ± 0.60 ppm to 124.59 ± 0.12 ppm (Table 6).

Table 6 The content of available silicon with collecting soil at various aged of the Rhizophora apiculata tree in Matang mangroves
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Discussion

Soil physicochemical properties

The pH was homogenous in the entire study area, so it could be categorized as slightly acidic because the pH value was just below 7. Previous results indicated that forests composed of Rhizophora apiculata had soil pH values of approximately 6.43 ± 0.12 (Satoru et al. 1994). Other research has documented those other flooded soils have pH values that are quite similar to that found in this study area (Hesse 1961; Clarke and Hannon 1967; De Laune et al. 1976). The range of pH values may be influenced by some major factors, such as the reductions in iron, manganese hydroxides, and carbonate concentrations, as well as the presence of carbonic acids and humic acids in mangrove soil (Ruttner 1963; Patrick Jr. and Mikkelsen, 1971). Soil salinity is generally characterized by the electrical conductivity (EC) of a soil solution, and a low EC can be influenced by the zonal distribution and season (Wakushima et al. 1993). Salinity is one of the most important drivers in the establishment and development of mangrove forests (Ball 2002). The results of this study confirmed that the soil salinity had been diluted with rainwater as the soils were taken during a rainy season in September 2012 and increase in freshwater run-off reduced the surface water salinity.

High CEC in Matang mangrove forest was influenced by high soil pH (Sukardjo 1994), and this situation is attributed to the accumulation of hydrogen sulfide in soil. However, when the this is exposed to air, mineral pyrites is oxidized to produce acid sulphate soil with a very low soil pH. Generally, a reflection of the organic matter and clay contents trend in soils increased the CEC with distance inland (Sukardjo 1994). The high CEC in Matang mangrove soil may reflect the large amounts of organic matter, suggesting that the soils potentially represent a large sink for cations that limit the availability of nutrients for uptake by mangrove trees (Sukardjo 1994). The soil fractions from the Matang mangrove forest were similar in terms of physical properties and texture class with previous results published by Sukardjo (1994). The dominant soil textures in the present study were classified as clay loam. Sand particles can be categorized as a moderate percentage of the soil because all the soil samples had less than 35% of sand particles, and this result suggests that the soil surface was mainly composed of small but newly deposited sediments, as described by Sukardjo (1994). The mangrove soil could be classified as clay even though the soil composition varied from organic peat to clay or sand (Soerianaraga 1971). We found that soil properties affect the ability of the mangrove pollutants by involved in their immobilization, such as adsorption of ion exchange sites for some nutrient, binding to organic matter and precipitation into insoluble compounds (Tan and Wong 1993).

Nutrient status of soil and roots of mangrove

One important factor in mangrove productivity is the availability of nutrients which are highly sensitive to variations in nutrient availability (Feller et al. 2003; 2013). We believed that reducing soil conditions and properties in the natural mangrove system are the factors that limit the nutrient concentration either in soil or mangrove trees themselves. The present study more focus on total N and available P because the most investigation of nutrient limitations to mangroves have focused on the macronutrients, such as N and P (Sukardjo 1994; Reef et al. 2010; Fred et al. 2013). These nutrients most likely limit the primary productivity of mangrove ecosystems (Krauss et al. 2008).

In roots, the oldest trees had more total N and available P compared to the youngest trees due to different amounts of biomass for each age level. Previous studies in Matang Mangrove Forest Reserve showed that different ages of mangrove trees (5, 10, 15, 20, and 25 years) had different amounts of their standing biomass with the average values ranging from 8 to 150 tons C ha−1 (Ong 1993). The oldest trees had larger standing biomass, which cannot accumulate more nutrients in their bodies. These findings also suggested that the oldest trees have a big root system to take up nutrients from the soil to the trees. It is presumed that a larger root system will enhance the uptake of nutrients and water by increasing the absorptive surface area (Peterson and Farquhar 1996). Because of these reasons, total N and available P concentration in the youngest productive area soil (5 and 10-years-old trees) was higher than in the oldest productive area (25-years-old trees) since there were lots of nutrients left in soils. Thus, the results indicated that the root system in mangrove trees plays a demonstrable role in nutrient uptake from the soil to the root. Total N is mainly a contribution from the decomposition of organic matter from mangrove plant parts and some organisms that encounter the area during tides and died. The same also occurred for the available P but less likely from the sea in origin. Since this area is situated in between two river tributaries, we may assume that it is coming from agricultural activity upstream of those rivers.

Total C in the Matang mangrove showed a decreasing trend (~4.5% changes) from the youngest production area to 15.21% in the oldest area. Our reported values are greater than the total C measured in a mature of an estuarine mangrove, Rhizophora mangle in subtropical, southeastern Brazil under pristine- (Cananéia, 5.2% ± 1.7) and impacted- (Cubatão, 12.6% ± 2.5) conditions (Sanders et al. 2014). The C determination protocol used in this study may contain C from organic matter and/or from carbonate-containing minerals. If we assume that total C is a direct contribution from mangrove plant parts, including leaves, flower, branches, and some organisms that are trapped in this area during water tide as organic matter. The mangrove forest is recognized as a very good C sequestration vegetation. The buried C in organic matter under the mangrove ecosystem resulted in from C sequestration is considered “blue C” (Rosentreter et al. 2018). This organic matter burial in mangrove forests results in the removal and long-term storage of atmospheric CO2.

Carbon to nitrogen (C:N) ratio is significant in composting process because microorganisms need a good balance of C and N (ranging from 25 to 35) to remain active. Our results showed that it ranged from 28 to 31 for all areas of mangrove production category. A high C:N ratio can lead to prolonged composting duration, and low C:N ratios enhance nitrogen loss. The higher C:N ratio in mangrove soils may be influenced by the soil fraction itself, which consisted of a large amount of sand and clay-sized particles. A similar finding was reported by Fred et al. (2013), who concluded that the high C:N ratio in mangrove soils is due to the accumulation of organic matter under anaerobic conditions in flooded soils. Therefore, anaerobic decomposition is a major contributing factor to the C:N ratios. The Matang mangrove soil had N limitation because it might be influenced by the denitrification process occurring in mangrove soils because there were many denitrifying bacteria in the soil samples. The results of another study suggested that the high rates of denitrification can deplete N sources in mangrove soils (Kristensen et al. 2008). In mangrove soil, the adsorption of ammonium was found to be lower than in terrestrial environment. This is because high concentration of cations from the sea water competes with ammonium for the binding sites required for N uptake by the plant (Holmboe and Kristensen 2002). Thus, the total N concentration of the mangrove forest is more concentrated in the soil and less so in the trees (Alongi et al. 2003).

This study measured only plant available P. This P fraction is commonly absorbed by plant roots. This value is considered a fraction of total P in the soil since the procedure did not consider occlude P and strongly fixed P- by Fe and Al ions in soil and also some organic P that is difficult to dissolve in this reagent. The ratio of N:P, recognized as the “Redfield ratio” is applicable to ocean plankton with respect to the macro-elements carbon (C), nitrogen (N), and phosphorus (P) were represented by 106C:16N:1P (They et al. 2017). In this study, N:P ratio was quite high in the soil of the youngest- (441:1) as compared to the oldest (381:1) productive area category of mangrove forests. The Redfield ratio has frequently been used in an ocean ecosystem. Based on the boundary of the N:P ratio of 16 (Redfield 1934), the greater N:P ratio resulted in P becoming limitation, and more production of N through microbial activity during the decomposition of organic matter in the mangrove forest production category. However, the decomposition of organic matter may occur through either aerobic or anaerobic organisms since the sampling areas are under the influence of tidal patterns.

The present study also focused on Si concentration since there were large amounts of Si, which was abundant in soil, where it acts as a “beneficial element” in the earth’s crust for mangrove tree growth (Marschner 1995). This study reported that only a minimal increase (2%) to 120.08 ± 4.04 mg/kg soil in available Si from the youngest to the oldest production category, in contrast for the same in mangrove roots was about 10% increase to 124.59 ± 0.12 mg Si/kg dry weight of roots. A high accumulation of Si may in the root of mangroves as compared to the soil may provide an interesting feature for the understanding of the Si transporter gene present in a mangrove tree root. A full-length cDNAs of 696 bp of serine-rich protein was cloned from a mangrove plant (Rhizophora apiculata) by amplification of cDNA ends from an expressed sequence tag homologous to groundnut (Arachis hypogaea), identified and submitted to NCBI (KF211374) (Sahebi et al. 2015). This is a serine-rich protein gene the encodes a deduced protein of 223 amino acids present in the root of a mangrove. High absorption of Si by roots and transported and accumulated in stem (Ani et al. 2011). Consequently, the wood of mangroves becomes very hard, especially roots, due to the presence of probably Si crystal (Fig. 2) in between water channels. With proper wood management practices, mangrove wood can be used for furniture (Hamdan et al. 2011).

Fig. 2
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Microscopy image of wood: a true mangrove (Rhizophora mucronate), b pores in between scalariform-pitted tracheids, c multiseriate staples and crystals (white round object), and d black mangrove (Brugeria gymnorrhiza) (after Ani et al. 2011)

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An abundance of Si in the soil may reflect a high Si concentration arising from the seawater from the incoming tide. These results are supported by a previous study by Kobayashi (1954) that showed high Si concentrations in rivers. Even though there were large amounts of available Si in the soils, not all could be taken up by the mangrove roots because they may face direct losses during the transportation process (Ma and Yamaji 2006). Moreover, the amount of Si available in the soil is also controlled by the soil pH. The soluble Si in the soil solution ranges from 1 mg/L to approximately 200 mg/L (Carlisle 1974). Although the mobility of Si in soils cannot be predicted accurately from the pH alone, soil pH has an especially marked effect on the Si concentration in the soil solution. Carlisle et al. (1974) found that increasing the soil pH to approximately 9 would decrease the Si concentration in the soil solution. The available Si in the soil solution should be less than the total Si adsorbed by ligand exchange onto the surfaces of iron and aluminum hydrous oxides (Russell 1963). The greater the surface area of the hydrous oxide and the higher the pH (up to 9.5), the more strongly the soil adsorb silicic acid, and the lower will be the concentration of Si in the soil solution (McKeague and Cline, 1963).

Conclusions

Variations in Matang mangrove root and soil nutrient concentrations were found in all categories of productive areas (youngest, immediate, and oldest). The C and N contents in the soil as indicated by the C/N ratio increases from 28 to 31 and P from 33.1 to 25.7 mg/kg soil in the youngest to the oldest mangrove ages. In contrast, the N and P content showed an increasing trend in the roots with the values from 0.24 to 0.36% and 0.06 to 0.10%, respectively from the youngest to the oldest mangrove ages. The same trend was also observed for Si. The nutrient status of the mangrove roots reflects the limitation of the returned and stored nutrients in the nutrient cycle with the age of standing mangrove trees in each productive area. The data obtained can be used by management practices for the enhancement of soil quality, such as by giving a proper amount of fertilizer to mangrove soil according to the productive area needed. Balance soil nutrient concentrations reflected in a better tree’s performance, established a greater forest ecosystem for wildlife conservation, economic value, and balancing environmental conditions.