MARINE CONTAMINANTS (beyond plastics) by Catherine Mouneyrac: University of Angers UCO 

Scientific background

Ocean pollution is widespread, crosses national boundaries and arises for more than 80% from land-based sources and anthropogenic activities. It reaches the oceans through rivers, runoff, atmospheric deposition and direct discharges. It is a complex mixture including chemical (organic and inorganic), biological (pathogens, viruses) and physical (nanomaterials, plastics, light, noise) agents which can interact amplifying their effects. Pollution is most highly concentrated along the coasts. Coastal eutrophication and acidification are one of the threats to the health of coastal social-ecological systems worldwide.

Ocean pollution has negative impacts on marine ecosystems and its threats to human health are great, but still incompletely understood. Over the past two decades, significant progress has been made in monitoring and detection (development of sensors, analytical techniques) of pollutants. Ecotoxicological studies has allowed advances in understanding sublethal effects, modes of action of pollutants at different levels of biological organization (molecular, organism, ecosystem) and growing knowledge of the “mixture effect” of multiple pollutants.  The interaction between climate change and marine pollution has been assessed on diverse species since increase of temperature is one of the major global issues, threatening the planet. 

Ocean pollution can be prevented. Like all forms of pollution, marine pollution can be controlled by deploying data-driven strategies based on law, policy, technology, and enforcement that target priority pollution sources. Restrictive regulations have been implemented such as the Grenelle de la mer (France), international conventions, such as the MARPOL, Stockholm Convention (Persitent Organic Pollutants  POPs) or the European Marine Strategy Directive. Successes achieved to date demonstrate that broader control is feasible. Heavily polluted harbors have been cleaned, costal and estuarine ecosystems restored. While significant progress is being made in understanding and mitigating ocean pollution, the scale of the issue requires a unified global effort combining science, technology, policy, and public engagement. 

Main Contributions of the French Communities through ANR (co)funding (Action plan and France 2030)

Over the last two decades, ANR has funded sixty-six projects on ocean pollution. The presence, fate and behaviour of contaminants in marine compartments as well as their impact on biota have been studied. A large variety of conventional and emerging contaminants (metals, POPs, nanomaterials, cyanobacteria, viruses), which pose significant risks to human health have been investigated. For example, the destruction of coral reefs in Pacific can be the cause of cyanobacterial blooms that produce toxins (anatoxin-a, ciguatoxin-like, palytoxin…) leading to human poisoning by seafood (ARISTOCYA). Eutrophication due to phosphorus inputs induced either by uncontrolled urban and industrial discharges or soil erosion led to the degradation of fishing and water supply areas (Vietnam) and is accompanied by toxic cyanobacterial blooms (DAY RIVER).

A huge effort in the development of devices has been performed to detect pollutants in the marine environment, such as metals (Lab-on-Ship), organic compounds (REMANATHAS), underwater sound waves (HYDRE) or cutting-edge technologies to deal with the consequences of pollution accidents, for example at a French nuclear reactor (PIA DECLIQ). Because adverse effects of chemical contaminants to the environment and humans have been widely described, the restoration of contaminated areas is a priority. Restoration with leguminous species had a positive effect on soil chemical quality highlighted by a positive effect on mercury speciation by reducing its mobility. (RIMNES). Concerning pollution by petroleum compounds, a transportable device for cleanup ships capable of detecting drifting oil slicks at sea has been proposed (DETHERPOLMAR) as well as detect oil spills with airborne surveillance radar (POLSHAR) The use of dispersant accelerate the attenuation of hydrocarbon contaminated mudflat sediments andd dispersed oil had no effect on the diversity of bacterial and macrofaunal organisms., Microbial communities of coastal sediments were involved in hydrocarbon degradation under real environmental conditions (DECAPAGE). The Gironde estuary, has been subjected for long time to industrial metal pollution from the Lot river (highlighted early in the 1970s). A remediation process was initiated on Riou-Mort watershed, a mining site contaminated by metals. The first impacts of remediation on periphytic biofilms, did not reveal a decrease of metal accumulation in biofilms revealing that recovery of aquatic communities after remediation can only be expected in the long term (RE-SYST). Remediation techniques of ecosystems contaminated by pesticides such as chlordecone in west-indies is a real challenge as well as for ecosytems than Humans.

Sentinel species of the water column (bivalve molluscs), widely used for the assessment of levels of contaminants (Mussel Watch programmes, Réseau National d’Observation de la qualité du milieu marin, Ifremer) as well as for examining their biological effects (International Council for the Exploration of the Sea) have been employed. Sediments are the final sink for most contaminants issued from human activities (metals, pesticides, hydrocarbons…). Following the earthquake and resulting tsunami in Japan in 2011, an unprecedented release of artificial radionuclides to the ocean from the Fukushima Daiichi nuclear power plants appeared. The nearshore sediments off Japan will remain a significant long-term source of radiocesium for years to decades (PIA AMORAD).

A guide of ecological risk assessment for the management of dredged sediments of ports has been proposed (SEDIGEST). Long-range atmospheric deposition also accounts for some of the variations in isotopic composition measured in the sediments. The coupling of Pb isotopes with Zn or Fe isotopes allows to identify and constrain the metal sources that contributed to sediment contamination (Artic metals). Endobenthic species (cockle, flounder, sole) exposed to sediment-bound contaminant, are also recognized as good models for biomonitoring purposes. Sediments also provide habitat, feeding and breeding areas for a number of benthic organisms. For example, a chronic pollution has been shown of the spawning grounds of the European sturgeon in the Garonne and more in the Dordogne and a contrasting toxicity of the sediments with respect to the sturgeon embryos and larvae (STURTOP). However, pollutant storage is not definitive and the contaminants can be remobilized and contaminate the water column for example of storms or dredging. The combined effects of contaminants and nutrients released from sediment into the water column during resuspension-mixing events were assessed on the phytoplankton composition and productivity in the anthropized lagoon of Bizerte (Tunisia). Results showed that sediment resuspensions are likely to have significant effects on the structure and productivity of pelagic primary producers. Lagoon site communities appeared to be more resilient (mechanisms of resistance) compared with those from a reference site (RISCO). Another study conducted at the Calanque National Park which constitutes one of the ten biodiversity hot spots identified in the Mediterranean basin and receives industrial and urban wastewaters discharged from Marseille and its suburbs. Results confirmed that PCBs and organochlorine pesticides in sediments induced toxic effect towards marine biota and more particularly for benthic communities (MARSECO). A special attention has been paid to endangered species such as eel or sturgeon to elucidate their toxicological status linked to populations decrease (ELL—SCOPE, IMMORTEEL, STURTOP). POPs are one of the suspected causes of this decline. Eels from the Gironde estuary confirmed the high level of PCBs in yellow eels’ muscle, and PBDEs contamination (ELL-SCOPE).  The use of species with a short life cycle, such as the zebrafish, a model widely used in ecotoxicology, allowed exposures starting with larva up to sexually mature adults. Detrimental consequences of exposure to PAHs were shown on fish performances and contribution to recruitment (CONPHYPOP).

In the environment are present a mixture of contaminants and their metabolites. Analyzing several classes of compounds present at trace or ultra-trace concentrations (ppb or ppt) requires the use of sophisticated apparatus and protocols. These requirements are very time-consuming, costly and some chemicals are not yet accessible for quantification. Therefore methodologies have been developed to estimate the average concentrations of pollutants in the environment taking into account the temporal variability of the contamination. Passive samplers (Semi Permeable Membrane Devices : SPMD, Diffusion Gradients in Thin film : DGT, Polar Organic Chemical Integrative Sampler : POCIS) are useful tools (ESMETOX). Assessing the impact of chemical pollution cannot be met on the basis of pollutant analysis alone since only a fraction of bioaccumulated chemicals can exert noxious effects on biota because of detoxification mechanisms in the organisms. Combining both biological responses and chemical analyses allows to identify toxic hot-spots, to characterize chemicals likely to cause adverse biological effects. The multi-biomarker approach based on sensitive and early warning signals providing information on the toxicity of mixture of pollutants on organisms has been extensively used over the last 30 years.  For example, atlantic cod were exposed to the water-accommodated fraction of different oils. PAH metabolites in bile confirmed exposure to and uptake of PAHs. Biomarker responses (CYP1A system and oxidative stress) in fish were able to discriminate among oil types and to monitor the environmental consequences of spills (AMPERA). Ecotox tests (applicable to high-throughput analysis), using marine embryos, have been proposed as useful tools for monitoring pollution (endocrine disruption, teratogenicity, genotoxicity) (MarineEmbryoTox). Combined biological and chemical-analytical approaches provide an important progress towards an estimation of the portion of an effect that can be explained by the analyzed chemicals. In this context, integrated strategies such as effect-directed analysis (EDA) are powerful tool to elucidate unknown causative toxicants in complex environmental samples and their combined effects, thus improving environmental risk assessment (ESMETOX). EDA showed that petrogenic components were responsible for the estrogen receptor and the androgen receptor mediated activity in north sea offshore produced water discharges. A guide to assess the impact of marine oil spills combining biological-effects techniques has been proposed. (AMPERA).

Studying low dose effects particularly in the case of exposure to mixtures constitutes a real challenge. Approaches helping to characterize the response of marine organisms to multi-contamination without preconception are key for understanding the impact of contaminants. Omics tools now make it possible to obtain considerably more complete and specific information on the biochemical response of organisms to biotic and/or abiotic stress. Environmental metabolomics, based on the identification of low molecular weight metabolites (50–1500 Da) whose production and levels vary with the physiological, developmental, or pathological state of cells, tissues, organs, or whole organisms has been applied to investigate deeply mechanisms and modes of action of contaminants. The response of mussels to waste water treatment plants effluents (pharmaceutical products) was characterized by the presence of a high quantity of modulated metabolites (e.g. amino acid, neurohormones, purine and pyrimidine metabolism, citric acid cycle intermediates (IMAP). Nowadays, there is still a controversy in whether environmental-induced changes in epigenetic marks (DNA methylation) can be inherited from one generation to the next. Cd exposure led to a progressive feminization of the population of fish (Danio rerio) across generations. A significant relationship has been shown between the methylation level of the foxl2a gene in mother gonads and the sex ratio of their offspring (TRACE). 

Metal pollution in the marine environment and their impacts have been regularly investigated on diverse species. Innovative tools (speciation, isotopes) were developed to discriminate metals sources (anthropogenic vs natural), mobility and reactivity and assessed their bioavailability for biota. The mechanisms involved in the production of the isotopically heavy Fe may lead this tracer to become a new indicator of environmental changes occurring in the boreal zone (Artic metals). Mercury, present under different chemical forms, along its biogeochemical cycle, can be accumulated and bioamplificated in aquatic food chains. Mercury speciation and stable isotopes fractionation in French Guiana highlighted the real impact of gold mining on native population (RIMNES). The consumption of seafood (Tuna), represents the main source of human exposure to methylmercury (main toxic form).  The first global maps of MeHg concentrations realized in different species of tuna for the global ocean, illustrates the geographical influence of anthropogenic mercury sources and the role of natural ocean processes (Mertox).

Among the POPs, emerging contaminants such as Pharmaceutical and Personal Care Products (PPCAs), Polybrominated Diphenyl Ethers (PBDEs) are ubiquist in the environment in the form of mixtures of different congeners (PEPSA). Antibiotics, antidepressants, and antifungals would deserve attention because of their ecological risk on marine ecosystems (Pharm@cotox). The long‐term effects of a diet exposure to mixtures of PBDEs and/or PCBs at environmentally relevant levels in zebrafish showed endocrine disruptions and an altered reproduction physiology. In the offspring, significant physiological, behavioural alterations and demographic effects (energy was reallocated from reproduction towards growth) were observed which added onto the altered offspring performances (Fish’N’POPs). 

The widespread use and release of nanomaterials in marine ecosystems is a concerning issue which has been also investigated. For example, the use of sunscreens leads to the release of nanoparticles in water. The quantification and characterisation of the released forms of by-products showed that nano-TiO2 UV filters rapidly loose their hydrophobic properties in contact with water and under light. Daphnia and Danio rerio were contaminated by sunscreen residues, but the stability of the external inorganic layer (AlOOH) of the nano-TiO2 UV filter lead to a strong decrease of the toxicity compare to bare Nano-TiO2 particles (AgingNano&Troph). There is today a strong demand (from both industry and consumers) for new innovations enabling the production of alternatives to current UV filters that are both renewable and safer.

The interaction between climate change and marine pollution has been assessed. Surface water temperatures at the spawning grounds of sturgeon have been shown that embryo-larval stages were very sensitive to temperature, and to a lesser degree hypoxia and chemical pollution (SturTOP). The influence of life history of species in the response to heat stress confirmed the vulnerability of populations to the increase in temperatures (IPOC). Highly contaminated flounders from the multi-contaminated Seine displayed a lower tolerance to thermal stress, compared to moderately contaminated fish from Vilaine (EVOLFISH). In the marine environment, bivalve mollusks constitute habitats for bacteria of the Vibrionaceae family. Differences in immune effectors could contribute to the higher resistance of mussels to infections (vibrios). Global warming and antimicrobial resistance (AMR) impact aquaculture as shown by infected aquatic animals presented higher mortalities at warmer temperatures (Labex Cemeb). Countries most vulnerable to climate change will probably face the highest AMR risks, impacting human health beyond the aquaculture sector.

In conclusion, ANR funded projects contributed to the structuring of the French (e.g. GDR Ifremer-INRA IMOPHYS : Integration of Molecular and Physiological responses to contaminants in coastal areas, Labex Cemeb) and international communities (e.g. France-Canada ECOBIM network, international joint laboratory : LMI COSYS-Med, IRD and the Tunisian Ministry of Research and Higher Education)  pooling of expertise teams (universities, organismes nationaux de recherche : CNRS, RD, INRAE, BRGM)  operating in the environment field (ecology, ecotoxicology, human health, biology, physiology, soil science, environmental chemistry, modelling). 

Research perspectives coming out of the ANR (co)funded projects 

Currently, 37 projects are in progress. The upgraded technology readiness levels and featuring enhanced metrological performance with the aid of AI and innovative accelerated numerical methods. This allows significant advances in pollution detection and monitoring in seas and high-risk zones such as coasts and ports. Currently, 10 projects aim developing new sensor technologies (e.g. radar, sensor equipped with a sampling drone to detect and monitor marine pollution (metals, phycotoxines, virus, pesticides, petroleum hydrocarbons, methane, nitrate, phosphate…). 

Better understanding marine ecosystem vulnerability (estuaries, coasts, coral reefs) to stress such as contaminants, acidification, eutrophication climate‐related environmental stress ; from individual responses to ecosystem health status assessment is always a real challenge. Despite long-term efforts, estuarine and costal ecosystems are impacted by several global change but only few are now in recovery. Coral reefs (4 projects) are well explored since critically endangered by anthropogenic stressors (chemicals, UV-filters, temperature, acidification), and the decline in many fish species needs understanding fish larval recruitment, a key step to preserve coral reef fish populations, improve their nutritional and safety quality because consumed by local populations. Generally, it is essential to better understand and predict the propagation of effects between trophic levels of marine systems.
One of the main issues in ecotoxicology nowadays is understanding the effects of exposure to pollutant low concentrations on organisms’ vulnerable life stages, life history, as well as their multi- and transgenerational effects. Recent works highlight the role of epigenetic alterations in mediating the response to environmental toxicant exposure. Massive gaps of knowledge is in understanding of toxicity (modes of action) of endocrine disruptive compounds. The potential of metabolomics  is powerful to highlight key metabolites disrupted by pollutants and then elucidate the biological effects of such exposure but there is  currently a lack of knowledge on metabolism of marine species. Addressing the combined effects of mixture of pollutants remains a significant challenge due to the complexity of interactions. There is a lack of knowledge of the occurrence, fate and toxicity of rare earth elements (e.g. lanthanides, indium, germanium), PPCPs, PFAs, pesticides (chlordecone) and their metabolites. Little research is conducted on the impact of noise and light on marine species, particularly in harbors. It is crucial to investigate putative disruption of the biological timing of marine organisms living in coastal environments and evaluate their consequences. It is also necessary to improve the ability of states to anticipate the future by producing reliable and robust ‘worst-case scenarios’ to overcome both technical and natural hazards such as industrial release, earthquake, a tsunami or a major nuclear accident.  

In conclusion, ocean pollution remains a critical global challenge requiring intersectorial (natural sciences and engineering, human and social sciences), interdisciplinary (ecology, ecotoxicology, analytical chemistry, sociology, law) and stakeholder expertise approaches. Prevention and remediation of ocean pollution creates many benefits. It boosts economies, increases tourism, helps restore fisheries, protect marine ecosystems (pollution-free marine protected areas) for future generations and improves human health and well-being.