Heavy metal pollution in coastal wetlands: A systematic review of studies globally over the past three decades

Highlights

• The first holistic systematic review of studies on heavy metal pollution in coastal wetlands globally.

• Research increased primarily in the USA before 2000 but China after 2010.

• Salt marshes and mangroves are better studied than seagrass beds and tidal flats.

• Multi-stressor interactions and remediation are among the fastest developing topics.

• Important areas (e.g., ecoremediation) for future research are highlighted.

Abstract

Coastal wetlands are ecosystems lying between land and ocean and are subject to inputs of heavy metals (HMs) from terrestrial, oceanic and atmospheric sources. Although the study on HM pollution in coastal wetlands has been rapidly developing over the past three decades, systematic reviews are still unavailable. Here, by analyzing 3343 articles published between 1990 and 2019, we provided the first holistic systematic review of studies on HM pollution in coastal wetlands globally. The results showed a trend of rapid increases in publications in this field globally, especially over the past ten years. Trends varied greatly among coastal countries, and global trends were primarily driven by the US before 2000, and in China after 2010. We also found that mercury (Hg), cadmium (Cd), and copper (Cu) were the most widely studied HM elements globally, but patterns differed geographically, with Hg being most widely examined in the Americas, Cd in China and India, and lead (Pb) in the western Europe and Australia, respectively. Among different types of coastal wetlands, salt marshes, mangrove forests, and estuaries were the most widely studied, in contrast to seagrass beds and tidal flats. As for ecosystem components, soils/sediments and plants were most extensively investigated, while algae, microbes, and animals were much less examined. Our analysis further revealed rapid emergence of topics on anthropogenic sources, interactions with other anthropogenic environmental changes (climate change in particular), and control and remediation methodology in the literature in the recent ten years. Moving forward, we highlight that future studies are needed to i) better understand the impacts of HM pollution in less studied coastal wetland systems and species, ii) deepen current understanding of the biogeochemical behaviors of HMs under anthropogenic activities, iii) examine interactions with other anthropogenic environmental changes, iv) conceive ecological remediation (i.e., “ecoremediation” as compared to traditional physiochemical remediation and bioremediation) strategies, and v) develop advanced analysis instruments and methods. The perspectives we brought forward can help stimulate many new advances in this field.

Introduction

Heavy metals (HMs), a group of elements with density greater than 5 g/cm³, including metals and metalloids such as cadmium (Cd) and arsenic (As), have been extracted from minerals and used by humans for millennia (Järup, 2003, Hou et al., 2020). In modern societies, HMs are used in a variety of industrial, domestic and agricultural processes, and their production and usage keep increasing (Hou et al., 2020). Over the past five decades, for example, global production of chromium (Cr) and lead (Pb) have increased by 514% and 232%, reaching 37.5 Mt and 11.3 Mt per year, respectively (British Geological Survey, 2019, Hou et al., 2020). Although HM concentrations can be naturally high in some regions due to geogenic sources and some HMs (e.g., copper [Cu] and Cr) are micronutrients, non-essential HMs and excess concentrations of essential HMs are toxic to living organisms (Antonovics et al., 1971, Schneider et al., 2013) Considering the stability, accumulation and biological amplification of HMs, the potential hazards of HMs have attracted global concern. Despite increasingly stringent environmental protection policies over the past few decades, HM pollution remains a major environmental problem in many regions, including developed countries (Yang et al., 2019). According to the most recent European Environment Agency (EEA) report, for example, about 75–96% of European seas are still contaminated with high levels of HMs (Andersen et al., 2019).

Some of the highly HM-polluted ecosystems are coastal wetlands located in the transitional zones between land and ocean, which include salt marshes, mangrove forests, seagrass beds, and tidal flats. Although coastal wetlands provide critical ecosystem services to human societies, including biodiversity maintenance, fishery nursery, carbon sequestration, and storm protection (Costanza et al., 1997, Barbier et al., 2011), they are subject to substantial inputs of materials from adjacent ecosystems, including HMs from terrestrial, oceanic and atmospheric sources (Fig. 1). Coastal human activities, such as agriculture, aquaculture, and sewage discharge, are associated with the use of artificial substances and fuels or production of waste and undesirable by-products containing HMs (Fig. 1; Pan and Wang, 2012; Gretchen and Edward, 2019). Inland discharge of HM pollutants can be transported over remote distances to coastal wetlands via water or air (Presley et al., 1980, Li et al., 2007, Gu et al., 2014). Furthermore, oceanic human activities, such as mining, transportation, and oil spills, produce large amounts of HMs that then deposit in coastal wetlands (Idaszkin et al., 2017, Ruiz-Fernández et al., 2019). Indeed, coastal wetlands have often been considered to be sorbents that remove HMs from coastal waters. Such a role can be particularly strong with the presence of aboveground and belowground vegetation structure and soils rich in organic matter (Simpson et al., 1983, Tam and Wong, 1996, Oliveira et al., 2018).

Some of the earliest studies on HM pollution in coastal wetlands date back to at least the 1970s. These studies documented increased Cd concentration in bivalves and sea skaters in coastal wetlands in the northwest Atlantic coast (Valiela et al., 1974) and Baja California, (Cheng et al., 1976), and investigated the distribution and transfer of HMs (e.g., Mn and Hg) and their driving environmental factors (Grieve and Fletcher, 1976, Windom et al., 1976). Early studies have also reported bioaccumulation and biomagnification of HMs in coastal wetlands, such as methylmercury in primary consumers in salt marsh estuaries of the southeastern Atlantic coast in Georgia, the US (Windom et al., 1976). Indices such as geoaccumulation index and enrichment factor were developed to assess the relative intensity/sources of HM pollution in sediments (Muller, 1969, Kemp et al., 1976). Observational and experimental studies were carried out to examine the toxic effects of HMs on living organisms. These studies have revealed that HMs can lead to the generation of free radicals, cause oxidative stress to organisms, damage their enzymes, proteins, lipids, and nucleic acids, including DNA, disrupt metabolic processes, and result in cellular and tissue dysfunction and even individual death (Nagajyoti et al., 2010, Jaishankar et al., 2014). Organisms resist HM stress and maintain homeostasis by enzymatic and non-enzymatic detoxification mechanisms, such as exclusion of HMs (e.g., via mycorrhizal association), binding with cell wall and excretion, metal chelation by phytochelatins and metallothioneins, and compartmentalization within vacuoles (Kushwaha et al., 2015). Those with strong detoxification capacities are often identified and utilized for HM remediation. These studies have also contributed to environmental regulations/laws that aim to monitor and control HM pollution. The US EPA, for example, adopted HM concentrations as a criterion for the evaluation of water quality including those in coastal wetlands in the 1980s. Biomonitors, including many coastal wetland organisms such as the algae Ulva lactuca, mussels of the genus Mytilus, and oysters of the genera Ostrea and Crassostrea, were proposed to be used to establish geographical and/or temporal variations in the bioavailability of HMs (Rainbow, 1995). More recently, an increasing number of studies have focused on control and remediation issues. Not only physiochemical but also biological remediation methods have been developed, with various hyperaccumulation plants (those with strong detoxification capacities) identified (Agunbiade et al., 2009, Verónica et al., 2018).

The study of HM pollution in coastal wetlands continues to prosper with its long and fruitful history. However, quantitative and systematic reviews of studies on HM pollution in coastal wetlands globally remain lacking. Existing reviews have been often descriptive and focused on a specific region, HM element, or type of coastal wetlands (e.g., mangrove forests, Kulkarni et al., 2018; seagrass beds, Bonanno and Martina, 2018). As research focus and funding often differ considerably among different coastal regions, whether research trends are consistent among different coastal regions/countries globally is unknown. Similarly, studies can vary according to HM elements, coastal wetland types (e.g., salt marshes, mangrove forest, or seagrass beds), ecosystem components (sediment/soil, water, plants, microbes, and animals), organization levels (physiological/individual, population, community, and ecosystem), pathways of HM migration and transformation (abiotic or biotic), and remediation methods (e.g., physical, chemical, or biological remediation). But how well are these specific areas investigated, how have these patterns changed, and what areas remain relatively understudied are still unclear. Given the rapidly mounting literature in this field globally, a systematic analysis of the global literature on HM pollution in coastal wetlands is thus primed to quantify research efforts and trends in different areas and identify gaps where research efforts need to be enhanced.

In this study, we provide a systematic review of studies on HM pollution in coastal wetlands globally over the past three decades between 1990 and 2019. Quantitative systematic reviews have the advantage of making use of information encompassed in the “big-literature” era (Nunez-Mir et al., 2016), and being inclusive and objective. Specifically, we addressed the following questions: (1) are research trends in this field over the past three decades consistent among different coastal countries globally? (2) what are the most and least studied topics and emerging trends regarding HM elements and their anthropogenic sources? (3) what are the most and least studied topics and emerging trends regarding ecosystem impacts of HM pollution and their control and remediation? Based on our literature analyses, we further outlined major knowledge gaps that may help stimulate new advances in how we understand and mitigate the detrimental impacts of HM pollution on coastal wetland ecosystems and the wellbeing of coastal societies.