The distribution of heavy metal in sediment and water
The data on Table 2 showed that the accumulations of (1) mercury were 0.1135–0.1559 ppm (sediment) and 0.0108–0.0166 ppm (water), (2) cadmium ranged from 1.25–1.96 ppm (sediment) and 0.0245–0.0339 ppm (water), and (3) zinc were 29.67–40.66 ppm (sediment) – 0.0455–0.0645 ppm (water). Based on the pollution category (Peraturan pemerintah no 82 2001), Hg, Cd, and Zn polluted the aquatic ecosystem in the Segara Anakan Lagon (SAL). Nour et al. (2019) records the data of heavy metal accumulation on the Red Sea coast and Egypt which Zn accumulation between 14.94–134.22 ug/g, Cd 0.12–1.25 ug/g, and Pb 3.17–40.25 ug/g. Alzahrani et al. (2018) reports that the mean concentrations of heavy metals in sediments are Cr (46.14 mg g_1 ± 18.48) > Cu (22.87 mg g_1 ± 13.60) > Ni (21.11 mg g_1 ± 3.2) > Pb (3.82 mg g_1 ± 2.46) > Cd (0.75 mg g_1 ± 0.87). According to Choi et al. (2020) potential heavy metal accumulation in Busan city has distribution that are Zn ≥ Pb > Cu > Cr ≥ As > Ni ≥ Cd > Hg. However, Hao et al. (2019) determine that the bioaccumulation of six heavy metals in China's Hainan and Zhoushan coastal regions including Cu, Pb, Zn, Cr, Cd, and Hg. Jeong et al. (2021) states that from the principal component analysis show that Cr, Ni, Cu, Zn, As, and Hg were derived naturally, while Cd and Pb were from anthropogenic sources..
Table 2 also showed that the potential heavy metal in sediment and water ecosystem had weak negatively correlation (a value < 0.5). However, the potential heavy metal in sediment still was higher than in the water ecosystem. According to Xin et al. (2014), 90% of heavy metals contaminants are high deposited in sediments. And (Chen et al. 2021a) and Barreto et al. (2016) also write that the organic materials and complex compounds were easily bound and deposited in sediments. Similarly, Cao et al. (2020) writes that heavy metal does not correlate with particle size, organic matter, or nutrients. Furthermore, heavy metal pollution give impact for water quality, including biological oxygen demand (BOD), chemical oxygen demand (COD), Oxygen demand (COD), pH, conductivity, total suspended solids (TSS), Kjeldahl nitrogen (TKN), ammonium (NH4+-N), nitrate (NO3−-N), and total phosphorus (TP) (Kibria et al. 2016; Xiao et al. 2019).
Basically, the highest of heavymetal accumulation occurred in mangrove vegetation, not in water or sediment, because the mangrove vegetation is used as a pathway to accumulate heavy metal ions from water and sediment (Kayalvizhi and Kathiresan 2019; Wang et al. 2019; Cao et al. 2020). But mangrove has metabolism system to reduceimpact of heavy metal pollution. The mangrove roots can stop transport non-essential matter or to accumulate in other dead organs.
The heavy metal contaminant in the sediment and water body is influenced by salinity, chemical oxygen demand (COD), and pH (Fig. 2). The station 3 had the highest COD score than others and is defined as a polluted area (COD < 25 ppm). Basically, mangrove ecosystem as a fragile ecosystem will be influenced by potential of heavy metal contaminant in water and sediment (Alzahrani et al. 2018). But, mangrove species still have an excellent adaptation to reduce potential heavy metal using excretion, excluder and accumulation gland (Hilmi et al. 2017b; Dai et al. 2017; Xie et al. 2020)
A disposal waste from oil refinery and cement industry is the main source of mercury contaminant. It is accumulated by a long-time deposition and binding process with organic matter (Xiong et al. 2018; Wolswijk et al. 2020). However, the accumulation in the sediment of E-SAL should be lower than the US EPA standard (< 0.2 mg/Kg). The largest cadmium accumulation in E-SAL comes from oil refinery activity. The oil refinery industry caused long cadmium deposition in the sediment and was distributed by tidal currents into the water column (Kibria et al. 2016; Analuddin et al. 2017; Liu et al. 2020b). Other sources of high cadmium accumulation include port and shipping activities (Karar et al. 2019). The Cd accumulation of sediment had an average of 1.60 mg/kg, more than the standard of (Canadian Environmental Protection Act 1999) (< 0.7 mg/ kg). Lin et al. (2021) established that Cd was the major contributor to health risk and social mortality. The greatest accumulation of Zinc (35.17 mg/kg) comes from the cement industry. However, its accumulation is lower than the (CCME (Canadian Council of Ministers of the Environment) 2001) (< 124 m /kg). This is still higher than (Riyanti et al. 2019) which focused on Payung Island South Sumatra (16.11 mg/kg).
In aquatic ecosystems (rivers and lagoon), mercury and cadmium accumulation had different significant distributions with Zinc accumulation. The decree of Peraturan pemerintah no 82 (2001) and Keputusan Menteri Negara Lingkungan Hidup NO 51 (2004) showed that their accumulation in the E-SAL was polluted because had exceeded the water quality standards for aquatic biota (Hg > 0.001 mg/L and Cadmium > 0.001mg/L). Ginting et al. (2019) suggest that the Tanjung unggat river estuary and Tanjung in Pinang City have Cd accumulation of < 0.001 mg/L, which was lower than in E-SAL (0.029 mg/L). However, Zinc accumulation in the aquatic ecosystem had less score than Peraturan pemerintah no 82 (2001) and Keputusan Menteri Negara Lingkungan Hidup NO 51 (2004) (Zinc < 0.1 mg/L), known as unpolluted. However, the heavy metal accumulation in E-SAL (0.055 mg/L) was still higher than (Ortega et al. 2017) with Zn accumulation of 0.003 mg/L.
The interpolation and distribution of total accumulation of heavy metal in mangrove ecosystem
The interpolation and distribution of total accumulation of heavy metal pollution in Segara Anakan Cilacap relative different with Jeong et al. (2021), because had concentrations of heavy metal in vegetation were 27–150 ppm (Zn) and 20–10 µg/Kg (Cd). Analuddin et al. (2017) demonstrated that potential high concentrations of Cu (83.85 µg g − 1) and Hg (0.52 µg g − 1) are found in the tissues of Lumnitzera racemose, while high concentrations of Cd (10.81 µg g − 1), Zn (70.41 µg g − 1), and Pb (1.36 µg g − 1) are found in the tissues of Bruguiera gymnorrhiza, Bruguiera parviflora, and Ceriops Tagal. Alzahrani et al. (2018) writes that the potential of heavy metals in Avicennia marina has range Cr > Cu > Ni > Pb > Cd (Analuddin et al. 2017; Liu et al. 2020a).
The heavy metals such as Hg, Cd, and Zn accumulation of mangrove vegetation on roots, stems, or leaves are bigger than in the water body but smaller than in sediments, because mangrove vegetations have ability to absorb, accumulate and use heavy metals from water and sediments following nutrient absorption to support their growth and metabolic processes (Analuddin et al. 2017; Zhang et al. 2019a). This metabolisms are influenced by root activity to absorb, transfer and translocate to other parts (Xiao et al. 2015; Alzahrani et al. 2018). Basically, mangroves also has ability to avoid death from heavy metal pollution, reducing toxic mechanisms using a dilution and translocation to dead or unnecessary tissues. Moreover, mangroves can increase organic matter absorption (Xiao et al. 2015; Nour et al. 2019). But, the heavy metals, such as Cd, Hg, and Zn,also significantly increase malonaldehyde and proline contents, inhibit photosynthetic pigment, and non-protein thiols, glutathione, and phytochelatins (Dai et al. 2017). de Almeida Duarte et al. (2017) find that metal contamination of Cd, Cu, Pb, Cr, Mn, and Hg in water, sediment, red-mangrove vegetation (Rhizophora mangle), and tissues.
Heavy metal accumulation in roots are higher than in stems and leaves because the roots function as a direct contact and nutrient absorber, followed by heavy metal absorption from sediment and water column (Analuddin et al. 2017; Nour et al. 2019) and then translocated to other parts (Hilmi et al. 2017b; Alzahrani et al. 2018; Chai et al. 2020). Similarly, MacFarlane and Burchett (2002) and Zhang et al. (2019a) established that the ion concentration of roots is higher than in the leaves and other parts. However, mangrove roots metabolize to avoid excessive heavy metal input, reducing the negative impacts on growth. The metal absorption is also influenced by roots’ absorption activity depending on the root system and their lenticels size (Ma et al. 2019; Mapenzi et al. 2020).
The main mangrove species, such as Sonneratia alba, Avicennia marina, and Nypa frutican, had the highest Hg accumulation. In contrast, Avicennia marina, Rhizophora apiculata, and Nypa frutican had the greatest Cd. Avicennia marina, Melaluca leucadendron and Xylocarpus granatum had greatest ability to accumulate Zn. Sonneratia alba, Avicennia marina, Nypa frutican, and Rhizophora apiculata dominated the first zone of the Segara Anakan (Hilmi et al. 2017b, 2019b, 2021c, a) and had both width spreading root (Hilmi et al. 2015) and a good respiratory system to grow in contaminant area. For example, the Avicennia marina had pneumatophore roots with a small diameter (< 0.9 cm) to absorb and reduce heavy metals pollution (Penha-Lopes et al. 2010; Sitoe et al. 2014).
The distribution of heavy metal accumulation in the mangrove ecosystem of Segara Anakan in Fig. 4 showed that average of heavy metal accumulation > deviation standard. The distribution of Hg accumulation between 0.020–0.032 mg/lt (average 0.025 and stdev 0.045 mg/lt). The distribution of Cd accumulation between 0..095–0.132 mg/lt (average 0.1155 and stdev 0.090 mg/lt). The distribution of Zn accumulation between 15.88–25.06 mg/lt (average 19.43 and stdev 5.48 mg/lt)
Moreover, the Fig. 5 must be correlated by critical condition of heavy metal pollution. The Zinc has a critical concentration classification with the deficiency ranging from 10–20 mg/kg. The healthy plants contain an amount of Zinc between 10–100 mg/Kg with an average of 60 mg/kg and toxic concentrations between 100–1000 mg/kg (Mertens et al. 2006; Wang et al. 2013; Robson et al. 2014; Kibria et al. 2016). Generally, Cadmium has a natural concentration in the soil between 0.1 mg/kg − 1 mg/kg, and human activities such as fertilization and industrial disposal can increase more than 0.1 mg/kg to 0.3 m/kg (Mertens et al. 2006; Wang et al. 2013; Kibria et al. 2016; Costa-Böddeker et al. 2020). The critical and toxicity of cadmium concentration in plants ranges from 10 to 20 ppm dry weight. Jiang et al. (2017) stated that mangroves had a response of phenolic metabolism to reduce the impact of Cadmium in plants. Mercury is toxic for many organisms, either as a single element or a compound (Li et al. 2016; St. Gelais and Costa-Pierce 2016). According to Mapenzi et al. (2020), the standard concentration of Mercury (Hg) was less than 0.2 mg/Kg. The toxicity symptoms of mercury affect plants, specifically chlorophyll damage, growth limitation, reducing membranes of root cells, photosynthesis, respiration, uptake of water, nutrients, and chlorophyll synthesis (Alzahrani et al. 2018; Zhang et al. 2019a).
Bioaccumalation factor (BAF) and Translocation Factor (TF) of heavymetal contaminant
Bioaccumalation factor (BAF) of heavymetal contaminant
The Table 3 give data’s that mangrove species has abilities to reduce impact of heavymetal with bioaccumulation process, namely 1) phytoextraction- the absorption ability of pollutants from water or soil through mangrove roots stored in plant canopy (Win et al. 2019; Yu et al. 2022), 2) Phytovolatilization- the absorption of pollutants using evaporative process and are transpired by mangrove leaves (McCutcheon et al. 2002; Zhang et al. 2019b), 3) phytodegradation or phytotransformation- the ability to absorb and destroy pollutants through the metabolism using enzymes or compounds (McCutcheon et al. 2002; Yang et al. 2008; Kagalkar et al. 2011), 4) phytostabilization- a pollutant transforming process into non-toxic compounds without absorbing process or keep these pollutants in soil (McCutcheon et al. 2002; Radziemska et al. 2021; Zhang et al. 2021), 5) rhizofiltration- the pollutant absorbing process by mangrove root on low pollutant concentrations (McCutcheon et al. 2002; de Oliveira et al. 2015; Yin et al. 2018)
According to Hilmi et al. (2017b), Analuddin et al. (2017) and Zhang et al. (2019a), BAF value ranges between 0 to > 1. A value > 1 indicates that the plants could accumulate contaminants because BAF has a positive correlation with ability to accumulate contaminant. This research showed that presence of Avicennia marina, Sonneratia alba, Nypa frutican, Rhizophora mucronata, and Rhizophora apiculata in the E-SAL was quite effective to accumulate heavy metals from waters, but mangrove doesn’t have the good ability to accumulate contaminant from sediments because mangroves still must have adaptation to live in pollution conditions (Analuddin et al. 2017; Shi et al. 2020; Chen et al. 2021b).
Translocation Factor (TF)
Translocation Factor (TF) is used to determine the metal transfer process and translocation from root to leaf. TF value > 1 shows that the plant can translocate the contaminants absorbed into the upper organs (Hilmi et al. 2017b; Analuddin et al. 2017; Shi et al. 2020; Chai et al. 2020). Mangrove root has an important role in preventing and reducing of heavy metal contaminants. However, the mangrove roots have ability to prevent the metal transport process and increase the accumulation of heavy metal contaminants (Jiang et al. 2017; Analuddin et al. 2017; Alzahrani et al. 2018; Chai et al. 2020).
The translocation factor correlates also showing the ability of heavy metal accumulation in stems and leaves. Avicennia marina, Rhizophora styles, Xylocarpus granatum, Sonneratia alba, Nypa frutican, Rhizophora mucronate, and Rhizophora apiculata have good hyperaccumulation system for reducing contaminants in water body and sediment. And give positive impact to reduce impacts of heavy metal on other living organisms (Alzahrani et al. 2018; Marambio et al. 2020)
Mangrove landscape based on heavy metal accumulation
The mangrove landscape showed that mangrove pioneers, that were Avicennia marina, Bruguiera gymnorrhiza, Sonneratia alba, Nypa frutican, Rhizophora mucronata, Rhizophora apiculata, and Xylocarpus granatum had high ability to reducing impact of heavy metal contaminant, because this species had function as phytoextraction, Phytovolatilization, phytodegradation or phytotransformation, phytostabilization, and rhizofiltration to eliminate lethal effects of heavy metal pollution (Syakti et al. 2013a; Costa-Böddeker et al. 2020).
The mangrove landscape was developed to protect the water system from land-based sources of pollution in the marine and coastal ecosystem and reduce toxic mechanisms using the dilution and translocation process (Ariani et al. 2016; Hilmi et al. 2017b; Analuddin et al. 2017). Additionally, zonation reduces the impact of malonaldehyde content, photosynthetic pigment, proline content, synthesis of non-protein thiols, glutathione, phytochelatins (Dai et al. 2017), yellow leaves (de Almeida Duarte et al. 2017), increase of lysosomal membrane integrity, cytogenetic and a pre-pathological condition (Shi et al. 2020).
The Clustering of heavy metal accumulation in mangrove ecosystem
This study showed that the mangrove ecosystem had 4 clusters, including Cluster 1- Melaleuca leucadendron, Xylocarpus granatum, Rhizophora styllosas, Aegicera floridum, Rhizophora mucronata, Cluster 2 - Ceriops tagal, Excoecaria agallocha, Rhizophora apiculata, Cluster 3 - Bruguiera gymnnorhiza, Nypa frutican, and Cluster 4 -Avicennia marina, Heritiera littoralis, Aaegiceras corniculatum, Bruguiera sexangula, Sonneratia alba. According Choi et al. (2020), Jeong et al. (2021), Yang et al. (2020) and Cao et al. (2020) note the clustering of heavy metal accumulation be influenced by rivers’ sites and surface sediment. The results showed that cluster 1 was dominated by silt and clay with high organic matter and nutrient concentrations. Cluster 2 contained rivers that were significantly affected by artificial pollution from heavy metals. Cluster 3 included sites with the lowest pollution effects caused by organic matter, nutrients, and heavy metals.