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Wei Guo, Xiaoyu Ji, Zhengfei Yu, Hongchen Jiang, Xiangyu Guan. Research Progress and Challenges on Persistent Organic Pollutants in Lakes. Journal of Earth Science, 2024, 35(2): 729-736. doi: 10.1007/s12583-024-1978-8
Citation: Wei Guo, Xiaoyu Ji, Zhengfei Yu, Hongchen Jiang, Xiangyu Guan. Research Progress and Challenges on Persistent Organic Pollutants in Lakes. Journal of Earth Science, 2024, 35(2): 729-736. doi: 10.1007/s12583-024-1978-8

Research Progress and Challenges on Persistent Organic Pollutants in Lakes

doi: 10.1007/s12583-024-1978-8
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  • Corresponding author: Xiangyu Guan, guanxy@cugb.edu.cn
  • Received Date: 02 Jan 2024
  • Accepted Date: 24 Jan 2024
  • Available Online: 11 Apr 2024
  • Issue Publish Date: 30 Apr 2024
  • Lakes are the main reservoirs of persistent organic pollutants (POPs) from land, atmosphere and rivers. POPs in lakes undergo complex exchange, transformation, and degradation between water-air-sediment-biota interfaces, which are constrained and regulated by various physical, chemical and biological factors. POPs can affect ecological conditions, chemical properties of water and sediments, and biodiversity of the lake system. Therefore, it is important to study the sources, migration, transformation, environmental behavior and ecological impacts of POPs in lake ecosystems. This review summarizes research progress on detection technologies, diversity and origins, historical records, migration and transformation, distribution patterns, degradation and toxic effects of POPs in lakes. Finally, future directions related to POPs in lakes were summarized.

     

  • Conflict of Interest
    The authors declare that they have no conflict of interest.
  • Persistent organic pollutants (POPs) have attracted considerable attention due to their potential toxicity, persistence, bioaccumulation, and long-distance transport (Melymuk et al., 2022; Jones, 2021; Sathishkumar et al., 2021; Ashraf, 2017). Traditional POPs mainly consist of polycyclic aromatic hydrocarbons (PAHs), organochlorine pesticides (OCPs), polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers, etc. Many countries have banned or restricted their use. For example, global annual consumption of pesticides is approximately 2 million tons. According to reports from the World Health Organization (WHO) and the United Nations Environment Program, about 200 000 people die from pesticides, and about 3 million people are poisoned every year (Yadav et al. 2015). In addition, there are some emerging POPs, such as long-chain perfluorocarboxylic acids (PFCAs), medium-chain chlorinated paraffins (MCCPs), and chlorpyrifos. Although they are not controlled by international conventions or regulations, they have also attracted extensive attention in the international community (Sonne et al., 2023; Ighalo et al., 2022).

    POPs can be roughly divided into pesticides and industrial chemicals according to their origin and into chlorinated, brominated and fluorinated types according to their chemical composition (Ighalo et al., 2022). Most POPs contain rigid benzene rings or heterocyclic structures, making their molecular configuration difficult to change; in addition, the covalent bonds between carbon and halogens are very stable, causing POPs molecules with more halogen elements to be more resistant to degradation (Aravind Kumar et al., 2022). However, under certain circumstances, POPs can also be broken down and transformed through abiotic and biotic pathways. For example, POPs in the atmosphere can be photolyzed by sunlight and free radicals. POPs in water and soil can be oxidized and broken down by microorganisms as carbon sources or energy sources (Heim and Schwarzbauer, 2012).

    POPs are widely distributed in the form of mixtures in the atmosphere, hydrosphere lithosphere, and biosphere and are migrated over long distances through the atmosphere or water systems (Liu et al., 2021). To date, high-level POPs have been detected in high concentrations in inaccessible areas such as Arctic, Antarctic and the Qinghai-Tibet Plateau, indicating their widespread distribution (Zhu et al., 2023; Morin-Crini et al., 2022). Lake ecosystems interact with the atmosphere, rivers, surrounding soils, and even the ocean. POPs can enter lakes through a variety of pathways, including river inflows and atmospheric deposition, and they are enriched by lake-specific environmental conditions such as high levels of organic matter and limited oxygen and light (Jane et al., 2021). Therefore, lakes are considered one of the ultimate reservoirs for POPs from land, atmosphere and rivers (Nava et al., 2023). Reconstruction of the POPS record in lake sediments can be used to map the historical impacts of associated human activities (Cheng et al., 2021; Ontiveros-Cuadras et al., 2019). POPs in lakes undergo complex exchange, transformation and degradation between water-air-sediment-biota interfaces, forming a complex cycling process that is constrained and regulated by various physical, chemical and biological factors (Aravind Kumar et al., 2022; Dadashi Firouzjaei et al., 2022). POPs can affect the ecological conditions, chemical properties of water and sediments, and biodiversity of the lake system (Aravind Kumar et al., 2022; Han and Currell, 2017). However, we currently have a limited understanding of the sources, migration, transformation, environmental behavior and ecological impacts of POPs in lake ecosystems, particularly awareness of the impacts of their transformation products. Therefore, studying the behavior and fate of POPs in lake ecosystems is of great scientific and ecological importance. This article reviews the research progress and existing problems of POPs in lakes and aims to provide theoretical reference for the monitoring, assessment, and control of POPs in lake ecosystems and the protection of ecosystems and human health.

    POPs are diverse in their composition and come from a wide variety of sources. POPs enter lake ecosystems primarily through agricultural runoff, urban runoff, glacial meltwater, and atmospheric deposition (Nava et al., 2023). POPs in many lakes, particularly near urban areas, come primarily from human sources, such as organochlorine pesticides, per- and poly-fluoroalkyl substances (PFAS) and PCBs produced by industry, as well as dioxins and furans from waste incineration and fossil fuel combustion. In addition, the lakes with less human influence also have a significant proportion of POPs from natural sources, including polycyclic aromatic hydrocarbons from volcanic eruptions, forest fires (Gorshkov et al., 2021; Zhang et al., 2020a), and microbial activities (Mojiri et al., 2019; Rocha and Palma, 2019; Pavlova et al., 2016).

    It is found that the compositions and sources of POPs in lakes are very complicated, which makes the detection and analysis of POPs in lakes very challenging (Meng et al., 2019; Bigus et al., 2014). In recent decades, various methods have been developed to trace the sources of POPs in lake ecosystems, including molecular diagnostic ratios and compound-specific isotopic analyses such as stable carbon (δ13C), hydrogen (δ2H) and radiocarbon (Δ14C) and receptor models such as principal component analysis (PCA), positive matrix factorization (PMF) model and chemical mass balance (CMB) model (Famiyeh et al., 2021). By tracking the sources and historical changes of POPs in lake sediments, the impacts of human activities, air pollution, volcanic activities, natural disasters, and other elements on lake ecosystems can be better understood.

    Lake sediment cores record the historical inputs and sources of POPs. POPs mainly occur as particles in sediments because most of them have lipophilic and hydrophobic properties, low solubility, and high affinity for organic matter. After entering the lake, most POPs settle to the bottom with organic particles and become bound in sediments. Over time, particulate matters deposit at the bottom of lakes, forming thick layers of sediments. They have high continuity and resolution and of course capture the historical distribution of POPs (Heim and Schwarzbauer, 2013). The content and distribution characteristics of POPs in lake sediments help us understand their primary sources and routes of entry. The sediment records of urban lakes primarily reflect direct inputs of POPs from wastewater and urban runoff, while the sediment records in remote lakes with less human activity reflect atmospheric transport and deposition of POPs (Ruiz-Fernandez et al., 2014). In addition, the sediment record of POPs may partially reflect the impacts and extent of human activities on lake ecosystems in different regions and time scales, including shifts in economic development and large-scale energy consumption, as well as the production, commercialization, and interdiction processes of POPs (e.g., PCBs, PBDEs) that have no known natural origins. For example, the shift in primary energy consumption from wood and coal to oil and gas associated with economic development has led to a change in historical trends in the concentrations of relevant POPs (PAHs, dioxins, furans, etc.) in lake sediment cores (Cheng et al., 2021; Zhang H X et al., 2019). Research on anthropogenic sediments typically focuses on sediments within a century, which requires high-precision dating methods such as 210Pb dating and optically stimulated luminescence dating. In contrast, sedimentary records of POPs from natural sources such as PAHs released by ancient forest fires need to be studied over a larger time scale. In this case, sediment dating uses techniques such as radioactive carbon isotope and paleomagnetics. POPs in lake sediment cores are also affected by a variety of other factors, such as sedimentation rate, organic matter content, and bioturbation. The authenticity and comparability of POPs deposition records need to be improved in the future through methods such as mechanistic studies and data correction. Studying the sedimentary record of POPs in lakes is of great importance for assessing the environmental risks of human activities in different time periods, formulating pollution prevention measures, and protecting ecosystems and human health.

    Figure  1.  The behavior and fate of persistent organic pollutants in lakes.

    The concentration of POPs is low in most lakes, so high-sensitivity detection technology is required. Although POPs are common in lake ecosystems, their concentrations are usually in the range of ng/L–g/L (Table 1). To monitor and assess the environmental risk of POPs, researchers have developed various methods for detecting POPs. Gas chromatography-Tandem mass spectrometry (GC-MS) and liquid chromatography-Tandem mass spectrometry (LC-MS) are currently the most common detection methods (Kuzmin et al., 2023; Gorshkov et al., 2022, 2019; Kustova et al., 2021; Zhang et al., 2020b; Guo et al., 2019). However, chromatography has inherent limitations such as a limited number of assays, expensive equipment, complicated measurement procedures and the inability to detect in-situ (Liu et al., 2023). To overcome these problems, some scientists began to try to use simpler and cheaper methods, such as fluorescence spectrometry, electrochemical methods, and other new testing techniques (Huang et al., 2022; Yao et al., 2019; Yang et al., 2018). However, these techniques also have some problems such as limited detection types, high detection limits and insufficient sensitivity. It turns out that there are still some technical limitations when testing POPs in lakes, and the monitoring and evaluation methods of POPs are not yet perfect. Therefore, more monitoring stations, sample libraries, and more accurate analysis methods need to be set up in the future. By determining the concentration of trace POPs in lakes, we can obtain information about the spatial and temporal fluctuations of POPs in lakes, thereby assessing the concentration, sources, and mechanisms of transport and transformation of POPs in the environment, as well as the impact of human economic and industrial development on global lake ecosystems.

    Table  1.  Content of persistent organic pollutants in the water and sediments of various lakes
    Lake Compounds Sample Range (mean) Instrumental analysis Reference
    Taihu Lake PFCs Water 17.8–448(51.8)a LC/MS Yang et al. (2011)
    PCBs Sediments 0.018–0.82b GC-MS Yin et al. (2017)
    OCPs Sediments 4.22–461b GC-MS Zhao et al. (2009)
    Dongting Lake OCPs Sediments 6.37–12.88(8.32)b GC-MS Wei et al. (2019)
    OCPs Water 1.25–6.02(2.91)a GC-MS Wei et al. (2019)
    PAHs Water 17.33–77.12a GC-MS Wang et al. (2016)
    PCBs Sediments 0.122 6–4.453 8b GC-MS Cui (2018)
    PCBs Water 0.077–10.321a GC-MS Cui (2018)
    Baiyangdian Lake PAHs Sediments 163.20–861.43b GC-MS Gao et al. (2018)
    OCPs Sediments 2.25–6.07b GC-MS Gao et al. (2018)
    PBDEs Sediments 0.231–1.224b GC-MS Gao et al. (2018)
    PCBs Sediments 5.96–29.61b GC-MS Dai et al. (2011)
    Guanting Reservoir OCPs Sediments 8.48–24.40b GC-MS Wan and Kang (2012)
    HCHs Sediments 1.11–7.73b GC-MS Wan and Kang (2012)
    DDTs Sediments 2.97–10.52b GC-MS Wan and Kang (2012)
    Reid Lake PCBs Water 42.33a GC-MS Bhardwaj et al. (2019)
    Mar Chiquita Lake PCBs Sediments 0.4–0.9b GC-MS Ballesteros et al. (2014)
    PBDEs Water 0.2–1.3a GC-MS Ballesteros et al. (2014)
    PBDEs Sediment 0.6–1.0b GC-MS Ballesteros et al. (2014)
    Lake Baikal PCBs Water 2684a GC-MS Samsonov et al. (2017)
    PCBs Sediment 1.7b GC-MS Samsonov et al. (2017)
    PAHs Water 52b GC-MS Samsonov et al. (2017)
    Caspian Sea PAHs Sediments 14.3–85.8b GC-MS Baniemam et al. (2017)
    PCBs Sediments 0.39–2.64b GC-MS Javedankherad et al. (2013)
    OCPs Sediments 1.8–12.68b GC-MS Javedankherad et al. (2013)
    a: ng/L; b: ng/g.
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    The intrinsic properties of POPs and environmental factors jointly determine their migration, transformation, and distribution patterns in lake ecosystems. These intrinsic properties include volatility, solubility, half-life, etc. (Ighalo et al., 2022). Once POPs enter the lake, easily soluble POPs migrate with the water flow, while poorly soluble POPs tend to be adsorbed on suspended particles and accumulate as the particles sink (Aravind Kumar et al., 2022). There is a likelihood that POPs with a longer half-life will be retained in lakes and are therefore more likely subjected to bioaccumulate (Zhang X M et al., 2019). The transport and distribution of POPs are also strongly influenced by environmental factors such as temperature, pH, and solar radiation intensity. Temperature is an important factor controlling the global transport and distribution of POPs. Temperature can affect the saturation vapor pressure of POPs and therefore the rate at which they escape from lake water into the atmosphere. POPs travel long distances in the atmosphere and are deposited on the Earth􀆳s surface, where they eventually "condense" in colder environments (Wania and Mackay, 1996, 1993). As a result, high-latitude, high-altitude and alpine lakes are becoming important sinks for atmospheric POPs worldwide (Jones, 2021). Changes in pH and ionic strength lead to changes in the charge state of POPs, which in turn affects their solubility and leads to adsorption or desorption at the water-sediment interface (Heim and Schwarzbauer, 2012). In addition, the redox potential of lake water and local solar radiation intensity will also affect the degradation rate of POPs, thereby influencing their stability and toxicity in lakes (Nadal et al., 2015; Cai et al., 2014). Studying the migration mechanism of POPs contributes to gaining an in-depth understanding of their behavioral patterns in lakes and also provides an important basis for environmental management and policy formulation.

    The degradation of POPs is mainly classified into abiotic degradation and biodegradation and is influenced by environmental factors. The abiotic degradation of POPs is dominated by photodegradation in the atmosphere, and its rate is influenced by the content of hydroxyl radicals (·OH) and ozone (O3) in the atmosphere (Ren et al., 2018; Wang et al., 2016). The current studies have shown that with increasing global warming, the atmospheric tropospheric ozone concentration increases, which enhances the photodegradation of POPs (Racherla and Adams, 2006). The microbial degradation of POPs mainly occurs in water and bottom sediments and can be divided into aerobic and anaerobic degradation. Aerobic degradation occurs in two ways: first, POPs are directly used by microorganisms as a carbon source or energy source, and this degradation occurs mainly through terminal oxidation (Pavlova et al., 2016; Ehrlich and Newman, 2010); second, POPs are degraded by microbial co-metabolism, which promotes the microbial degradation of POPs by adding appropriate compounds as carbon sources (Juhasz and Naidu, 2000; Bouchez et al., 1995). In contrast, under anaerobic conditions, halogen-containing POPs such as HCB and DDT are more easily degraded through dehalogenation due to their higher redox potential (Ruan et al., 2020). Some aromatic compounds are broken down anaerobically through hydration and dehydrogenation (Ehrlich and Newman, 2010). It is worth noting that the direction of change in the toxicity and stability of the degradation products of POPs remains unknown. For example, the desnitro/guanidine intermediate derived from microbial degradation of imidacloprid is approximately ten times more toxic than imidacloprid (Pang et al., 2020). Chlordane epoxide, which is produced by microbial degradation of heptachlor, is more toxic and stable than heptachlor (Qiu et al., 2018). The degradation process of POPs is a dynamic process, whose interactions and feedbacks with environmental factors must be taken into account. Therefore, studying the degradation mechanisms and patterns of POPs in lake ecosystems is of great importance for assessing their environmental risks, controlling the spread of their pollution, and formulating effective management measures.

    POPs affect human, animal and plant health to varying degrees in multiple pathways. In lake ecosystems, plants and animals are directly or indirectly exposed to environments contaminated with POPs. POPs accumulate in organisms and disrupt their normal functions, leading to disease, death, and reproductive disorders. According to the U.S. Environmental Protection Agency, exposure to POPs can result in unusually high rates of morbidity and increased mortality in wildlife such as certain fish, birds, and mammals (Han and Currell, 2017). After POPs accumulate in lake organisms, they will affect the health of the organisms by affecting gene arrangement, gene expression, and normal hormone secretion (Sanganyado et al., 2021; Tkaczyk et al., 2020; Sharma et al., 2014). Previous studies show that POPs can damage the immune, nervous, and reproductive systems of a variety of organisms (fish, shellfish, algae, etc.) in lakes, which can manifest as intestinal damage, metabolic disorders, etc. (Li et al., 2023; Han and Currell, 2017; Wan et al., 2015). Lakes serve as important sources of water supplies and aquatic products. Long-term drinking of untreated lake water or consumption of lake aquatic products contaminated with POPs can also have toxic effects on human health. Almost all POPs originally named in the Stockholm Convention have been detected in breast milk in several countries, and excessive exposure to POPs can cause damage to multiple organs in humans, including the liver, intestines, and brain (Chinnadurai et al., 2022; Sathishkumar et al., 2021; Fernandes et al., 2019; Li et al., 2019). Therefore, long-term excessive exposure to POPs can have serious negative impacts on ecosystems and human health. The existing environmental management regulations (e.g., "China Drinking Water Quality Standard" (GB 5749-2022) mainly restrict traditional POPs such as pesticides, but do not contain clear restrictions on emerging POPs. In addition, the long-term ecological risk of POPs in lake ecosystems remains unclear, and the relevant ecological risk assessment methods and standards are not well developed. There are numerous challenges in protecting the biodiversity and environmental quality of lake ecosystems and in managing the ecological risk of POPs.

    POPs pollution is one of the biggest environmental problems. As important sinks of POPs, lakes are key nodes in the global migration and transformation of POPs. Studying POPs in lake ecosystems is helpful in understanding the fate of POPs. However, research on POPs in lake ecosystems still faces many challenges, such as the complexity of traceability, the heterogeneity of distribution, the diversity of transport and transformation pathways, the unknown degradation mechanisms, and the inconsistent standards for ecological risk assessment (Jones, 2021). Future research on POPs in lakes needs to further investigate the relevant in-situ detection technology, traceability, migratory behavior of POPs, and the environmental impact and ecological risks of the transformation intermediates of POPs in lakes. The details are as follows:

    Develop more accurate methods for dating sediment cores and tracing the sources of POPs. Many challenges remain in incovering historical changes and sources of POPs in lake ecosystems and in assessing the impacts of human activities. Existing source apportionment methods are not sufficient to identify mixed sources of POPs (Famiyeh et al., 2021). There is an urgent need to develop more advanced and accurate methods that combine various environmental indicators and address the degradation and transformation processes of POPs. Furthermore, when examining sediment records, the effects of factors such as hydrodynamics, biological disturbances and organic matter content are rarely considered (Heim and Schwarzbauer, 2012). There is an urgent to improve correction methods for lake sediment records and to increase the accuracy and resolution of sediment dating.

    Developing efficient, accurate, and practical detection methods /technologies and associated devices/instruments. Current POPs detection methods have inherent drawbacks such as limited detection capacity, cumbersome sample processing, high cost, and inability to detect in-situ. For example, there are approximately 5 000 different PFAS in the environment, but current available characterization methods mainly focus on perfluorooctane sulfonate and perfluorooctanoic acid (Dadashi Firouzjaei et al., 2022). In order to detect more unknown and neglected POPs, the following measures are suggested to be taken: the targeted and non-targeted detection methods are combined to improve the comprehensiveness of detection methods; the existing sampling and pretreatment methods are optimized and improved to reduce contamination and interference; and new technologies such as nanotechnology and biotechnology are employed to reduce detection cost and environmental impact and to achieve in-situ detection ability.

    In-depth study of control methods for migration processes and the fate of POPs in lakes. Exploring on the migration mechanism of POPs in lakes is the basis for understanding the ecological risks of POPs. In the future, interdisciplinary techniques such as molecular biology and isotope tracing can be combined with laboratory and field research to study the micro- and macro- mechanisms of migration behavior of POPs in lakes, such as the exchange mechanism of POPs between gas-water-particles and the plant absorption mechanism of POPs in water. This can provide theoretical support for the predicting and controlling POPs migration in lakes (Aravind Kumar et al., 2022; Göktaş and Macleod, 2016). Current research on POPs in lakes is mostly limited to a few typical lakes or regions and ignores comparisons between lakes of different types and regions (Ruiz-Fernandez et al., 2014). Lakes studied in the future should consider factors such as their geographical regions, climate types, pollution levels, environmental conditions, etc. Furthermore, microbial activities play an important role in the migration and transformation of POPs in lakes. The mechanism of microbial degradation of POPS in lakes awaits further investigation.

    Microbial degradation mechanism and its influencing factors of POPs in lake ecosystems. It is necessary to analyze the interaction between lake community structure and POPs, screen and isolate microorganisms capable of degrading POPs, analyze their degradation pathways, products and efficiency, study their degradation mechanisms and regulatory factors, and create a kinetic model of the microbial degradation of POPs. Furthermore, the following aspects are also to be investigated: the impact of microbial degradation of POPs in lake ecosystems, such as the toxicity of degradation products, the energy metabolism of degradation process, and the ecological adaptability of degradation strains. The abovementioned studies will reveal the natural degradation process of POPs in lakes and the corresponding microbial mechanisms, and provide theoretical foundations and technical support for the bioremediation and ecological restoration of POPs in lakes.

    Optimize existing methods for assessing ecological risk and biotoxicity of POPs. To effectively assess the ecological risk and biotoxicity of POPs, the following measures should be taken: select biomarkers at different levels, such as molecules, cells, tissues, individuals, and populations, assess the acute and chronic toxicity and bioaccumulation of POPs and their transformation intermediates to lake organisms and reveal their effects on the physiology, genetics, and behavior of lake organisms, and assess the potential hazards of POPs in lakes to aquatic life and human health (Aravind Kumar et al., 2022). With the help of computer modeling and other technical means, the following measures can be taken: comprehensively consider the exposure level (Liu et al., 2021; Zhang et al., 2019), biological impacts, ecological sensitivity and receptor susceptibility of POPs in lakes, evaluate the impact of POPs on the structure and function of lake ecosystems, predict the impact of POPs on lake ecology and human health, and provide scientific basis and policy recommendations for pollution prevention and risk management of POPs in lakes. Moreover, the chronic effects of POPs in lake water on human health needs to be studied by monitoring the health status of surrounding residents for a long period of time. To ensure the safety of water sources, drinking water treatment technologies that can effectively remove POPs must also be developed.

    ACKNOWLEDGMENTS: This work was supported by the National Natural Science Foundation of China (No. 42172336). The final publication is available at Springer via https://doi.org/10.1007/s12583-024-1978-8.
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