Antimony uptake by mangroves and its environmental fate in the Sundarbans, India

https://doi.org/10.1016/j.ecss.2020.106923Get rights and content

Highlights

  • Sb stock is determined in mangrove biomass and sediment.

  • Sediment of the Sundarbans mangrove is the largest reservoir of Sb.

  • Sb budget reveals strong sink capacity of the mangroves.

  • Sb is recycled within the organic pool of the mangroves.

  • Pollution indices reveal safe level of Sb in the mangrove ecosystem.

Abstract

Antimony (Sb), a naturally occurring trace element, tends to be enriched in the top-soil and contributes to soil contamination due to continued human activities. However, little is known about plant uptake of Sb, its storage in plant biomass and recycling in large littoral zones of tropical regions, subjected to strong anthropogenic impact. Biogeochemistry of Sb has been studied in the world's largest Sundarbans mangroves by measuring Sb concentration in sediment, plant organs, river water, sea water and pore water, and by determining Sb fluxes within the ecosystem reservoirs. Mangrove estuarine water and sediment appeared to be non-polluted in Sb as confirmed by their ecotoxicological indices. Sediment represented major pool of Sb (2170 g ha−1) compared to plant biomass (2.2 g ha−1). Antimony concentration (μg kg−1) in mangrove roots was highest (17 ± 6) followed by leaf and wood (10.5 ± 6, 9 ± 4, respectively, n = 24). Species-specific variability in Sb concentration was observed with Aegiceras corniculatum, showing highest concentration (48.8 μg kg−1) and Avicenna marina lowest (16.6 μg kg−1). Riverine input of Sb (9.3–12 Mg yr−1) was 3-order of magnitude higher than the mangrove sediment-derived input (0.02–0.05 Mg yr−1), suggesting the latter as negligible contributor of Sb to the Sundarbans coastal water. The mass balance calculations demonstrate that 63–88% of the annual riverine discharge of Sb export to the Bay of Bengal. Further biogeochemical studies should address Sb transport and speciation in surface waters and pore waters of this region.

Introduction

Antimony (Sb), generally a non-essential toxic metalloid, is widely distributed in the Earth surface environment as a result of natural (rock weathering and soil runoff) and anthropogenic (fossil fuel combustion, mining and smelting activity, vehicle emission, fertilizers for agriculture) factors (Nash et al., 2000; Filella et al., 2002, 2009). Antimony belongs to group Va of the periodic table, and usually occurs in +III and occasionally in +V oxidation state along with organic form methylstibonic and dimethylstibonic acid (Baes and Mesmer, 1976), and shows amphoteric behavior. Redox sensitive Sb has two positive oxidation states (III and V) which are predominant in natural environmental condition. Antimony is a strong chalcophile and mainly occurs in nature as Sb2S3 (stibnite, antimonite) and Sb2O3 (valentinite). These compounds are generally found in ores of copper, silver, and lead. The reduced oxidation state of Sb (III) is reported to be 10-fold more toxic than its (+V) state because Sb (III) is able to reach critical biological targets (Filella et al., 2002; Fowler and Goering, 1991). Antimonite, Sb (III)-oxidizing bacteria can transform the toxic Sb (III) into the less toxic antimonate Sb(V) (Li et al., 2017). Sb (V) is the predominant oxidation state under oxic condition in contrast to Sb (III) which is more stable in the aquatic suboxic or anoxic environment. The anthropogenic release of Sb to the environment stems from using it in the Sb–Pb alloys, and from recently emerged application in microelectronics (i.e. semiconductor materials).

The crustal abundance of Sb is low (<1000 μg kg−1) except argillaceous sediments which contain up to 2000 μg kg−1 (Fowler and Goering, 1991), and it is concentrated in soils (<3000 ± 8400 μg kg−1) as compared to rocks (Crommentujin et al., 1997). In human tissue, Sb is usually present at levels less than 1000 μg kg−1 (Fergusson, 1990). Concentrations of Sb vary widely in world estuaries (484 ± 522 ng L−1) but generally remain stable in ocean water (184 ± 45 ng L−1) (Filella et al., 2002). Dissolved inorganic Sb displayed mildly scavenged behavior that was confirmed by correlations with aluminum, but atmospheric inputs that may be anthropogenic in origin also affected its concentrations (Cutter and Cutter (2006). According to the Council of European Union (1998), permissible limit of Sb in drinking water is 5000 ng L−1. This range can be exceeded at times due to local input or mobilization of Sb from soil, thus poses hazards to human health.

In a growing industrial activity context, pollutants are released into the coastal marine water via estuaries and wetland waters, leading to undesirable consequences on the marine ecosystem (Liu and Su, 2017; Ahmed et al., 2019). Antimony is released to the aquatic environment as a result of soil run off, rock weathering and anthropogenic activity. In highly polluted areas like in a Sb mining area of Italy or tin deposit mountain of China, soil Sb concentrations exceed its natural abundance 1000 times, reaching up to 2000 to 4400 (mg kg−1) (Cidu et al., 2014; Wang et al., 2010). Antimony is considered as a nonessential element and is known to be easily absorbed by plant if present in soluble forms. Bowen (1979) reported a Sb mean of 60 μg kg−1 in land plants. As a natural measure against toxic effects, Sb in soil pore water can be sequestered by plants such as rice and maize (see Feng et al., 2013). Former reviews (Filella et al., 2009; Wilson et al., 2010) and recent works (Fawcett et al., 2015; Fu et al., 2016) suggest that despite high concentration, the mobility of Sb in contaminated soils is considerably low, being lower than that of arsenic (As). Knowledge of speciation and physicochemical state of Sb is important for understanding its behavior in the environment and its availability to biota. Mobility and sequestration of Sb in marine and wetland sediment were addressed in various studies (Migon and Mori, 1999; Chen et al., 2003; Sharifi et al., 2016; Warnken et al., 2017; Mandal et al., 2017), however, there is no evidence of bioconcentration of Sb in marine plants, particularly in mangroves.

Mangroves, a major wetland located across tropical and subtropical regions play a vital role as a major primary producer in the estuarine ecosystems (Kristensen et al., 2008; Alongi, 2014). Despite their importance in ecosystem functioning (such as carbon sequestration, barrier against extreme coastal hazards, aquaculture and food resources), mangrove ecosystems have experienced significant contamination, aggravated by rapid urban development (Agoramoorthy et al., 2008). The mechanisms of metal accumulation and removal in mangrove plants have been poorly documented (Marchand et al., 2016; Alzahrani et al., 2018; Thanh-Nho et al., 2018), and in contrast to As (Mandal et al., 2019a), the biogeochemical cycle of Sb in coastal environments is not well understood (Cutter et al., 2001). Here, we hypothesized that mangroves could be a potential sink of Sb while storing it within the biomass and soil/sediment reservoir where a major fraction of stored Sb would be recycled within the organic structure of the vegetation.

For the present study we explored the Sundarbans, a largest deltaic mangrove patch on Earth. The Sundarbans mangroves play a key role in conservation of north east coastlines of the Bay of Bengal (India), notably acting as a buffer between the land and coastal waters. Like other mangroves, the Sundarbans support a wide variety of ecosystem services, such as accumulation of metals and metalloids by trapping suspended material from the water column, and because of their richness in organic matter (OM), various sedimentary OM diagenetic processes make them true natural biogeochemical reactors (Ghatak et al., 2004; Banerjee et al., 2012; Mandal et al., 2013). Now, Indian part of the Sundarbans and associated Hooghly river estuary suffer from past environmental degradation due to anthropogenic pressures such as, tourism, port activities, operation of excessive number of mechanized boats, mangrove poaching, agricultural and aquaculture practices. As a result, the presence of inorganic and organic pollutants in the Sundarbans sediments have been reported in previous geochemical studies (Antizar-Ladislao et al., 2015; Chatterjee et al., 2009), but those exclude any such data on Sb. Previously, we quantified Sb concentration in river/tidal water, ground water, and pore water of the Sundarbans (Mandal et al., 2011), but Sb concentration profile in sediment cores and the role of mangroves in sequestering Sb into biomass have not been examined yet despite their implications in reducing Sb pollution level and acting as a safe guard for the local habitats. This study contributes to better understanding of metal and metalloids contaminations and distributions in the waterways of Sundarbans mangrove and suburban areas.

Therefore, our research objectives are: (1) to estimate stock and turnover of total Sb (III and V) in mangrove biomass and sediment, (2) to examine pathways of Sb delivery into the Bay of Bengal, and (3) to determine the toxicity and pollution index of Sb for the entire ecosystem.

Section snippets

Study area

The Indian Sundarbans mangrove (210 32–220 40/N, 880 05/–890 E) located in the estuarine phase of the river Ganges, NE coast of Bay of Bengal, extend over 9630 km2, out of which 4264 km2 is of inter tidal area covered with dense mangroves, and 1874 km2 is of aquatic ecosystems. Aquatic ecosystems comprise 891 km2 as river water domain (close to blind rivers, creeks, canals) and 983 km2 as tidal influenced aquatic area (Ray et al., 2018). In 1984, a subordinate protection of the forests came

Occurrences of Sb in the Sundarbans mangroves

Antimony concentrations (μg kg−1) varied widely among different environmental matrices (Fig. 2), such as sediment (280–830, n = 15), plant leaf (4.4–22.5, n = 8), wood (2.3–12, n = 8), and root (2.6–26.4, n = 8). Previously, we observed varying degree of Sb concentration in suspended particulate (80–190 μg kg−1, n = 10) and dissolved forms (ng L−1) such as tidal water (230.8–303.1, n = 60), pore water (375.5–590.9, n = 36), ground water (250.0–327.5, n = 8), and river water (683–780, n = 10) (

Conclusions

Mechanistic studies of Sb biogeochemistry in anoxic wetland sediments are scarcely available. This study fills this gap via quantifying potential role of Sundarbans mangroves in Sb sequestration in the sediment and plant biomass and estimating exchange fluxes of Sb within the ecosystem reservoirs. Vertical profile of Sb distribution indicated its accumulation within the deeper anoxic sediments that might be related to its removal from porewaters by physico-chemical processes, such as

CRediT authorship contribution statement

S.K. Mandal: Writing - review & editing. R. Ray: Writing - review & editing, Writing - original draft. A.G. González: Writing - review & editing. O.S. Pokrovsky: Writing - review & editing. T.K. Jana: Writing - review & editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgement

Authors sincerely thank V. Mavromatis (GET, Toulouse) for providing instrumentation and measurement in ICP-MS. SKM was supported by University Grant Commission, New Delhi with a minor research project (No. F, PSW-076/13-14, ERO). RR and AGG thank the postdoctoral grant from the LabexMER International Postdoctoral Program, Laboratoire d'Excellence LabexMer, and Universidad de Las Palmas de Gran Canaria. Authors are grateful to the Sundarbans Biosphere Reserve for giving permission to undertake

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