Human Health and Ocean Pollution

Releases of toxic metals to the environment began millennia ago with the inception of mining and smelting. These releases have increased since the beginning of the Industrial Revolution and risen especially in the past two centuries [58,59,60].

Mercury is the metal pollutant in the oceans of greatest concern for human health [34]. Over the past 500 years, human activities have increased total environmental mercury loading by about 450% above natural background. About 70% of the mercury circulating in the environment today consists of mercury emitted from human sources in the past, termed legacy mercury [61] (Figure 3). The presence of large quantities of legacy mercury in the global environment and the potential for climate change to remobilize this mercury complicate projections of future exposures and health impacts.

An estimated 2,220 tons of mercury are currently emitted to the environment each year as the direct result of human activity. These emissions account for about 30% of current mercury emissions. Another 60% of current mercury emissions result from environmental recycling of anthropogenic mercury previously deposited in soils and water. The remaining 10% comes from natural sources such as volcanoes.

Combustion of coal and artisanal/small-scale gold-mining (ASGM) are the two principal human sources of current mercury emissions. All coal contains mercury and when coal is burned, mercury is released into the atmosphere where it can travel for long distances until ultimately it precipitates into rivers, and lakes and the oceans.

In ASGM, mercury is used to form an amalgam to separate gold from rock. The amalgam is heated to boil off the mercury leaving the gold behind. ASGM operations release mercury to the environment through vaporization and through runoff of spilled mercury into waterways [34]. Metal mining and oil and gas exploration can be additional sources of mercury release. In rivers, lakes and the oceans, the metallic, inorganic mercury released to the environment from these sources is converted by marine microorganisms into methylmercury, an organic form of mercury that is a potent neurotoxicant.

The largest fraction of global mercury emissions – about 49% – originate today in East and South-East Asia. Coal combustion and industrial releases are the major sources there. South America accounts for 18% of global mercury emissions and Sub-Saharan Africa for 16%. In both of these regions, ASGM is the major source of mercury releases.

Methylmercury is a persistent pollutant in the marine environment. It bioconcentrates as it moves up the food web, so that top predator species such as tuna, striped bass and bluefish as well as marine mammals can accumulate concentrations of methylmercury in their tissues that are 10 million or more times greater than those in surrounding waters [34].

Mercury levels vary substantially in different regions of the ocean. This variation is seen in a recent survey of methylmercury concentrations in yellowfin tuna, in which levels differed by 26-fold around the world. Highest levels were found in tuna from the North Pacific Ocean (Figure 4), and these high concentrations reflect mercury releases from coal-fired power plants and steel mills in Asia that are carried northeastward across the Pacific on the prevailing winds [62,63].

Human exposure to methylmercury occurs primarily through consumption of contaminated fish and marine mammals [34,64] Populations in the circumpolar region are heavily exposed to mercury in their diets – principally in the form of methylmercury – as a consequence of their traditional consumption of a diet rich in fish and marine mammals. Most of the mercury to which these populations are exposed originates from sources far away.

The brain is the organ in the human body most vulnerable to methylmercury. This vulnerability is greatest during periods of rapid brain growth – the nine months of pregnancy and the first years of postnatal life [65].

There appears to be no safe level of methylmercury exposure in early human development.

Prospective epidemiological cohort studies undertaken in the Faroe Islands demonstrate that children exposed to methylmercury in utero exhibit decreased motor function, shortened attention span, reduced verbal abilities, diminished memory and reductions in other mental functions. Follow-up of these children to age 22 years indicates that these deficits persist and appear to be permanent [66].

A similar study conducted in Nunavik of child development at age 11 years showed that methylmercury exposure in early life is associated with slowed processing of visual information, decreased IQ, diminished comprehension and perceptual reasoning, impaired memory, shortened attention span, and increased risk of attention deficit/hyperactivity disorder (ADHD) [67,68]. Other prospective studies have also reported neurobehavioral deficits in children with elevated prenatal exposure to methylmercury [69].

Mercury exposure later in childhood and also in adolescence can also cause damage because the human brain continues to develop throughout this time [70]. Genetic factors may increase vulnerability to methylmercury in some individuals [71].

Recent studies have shown that adult exposures to methylmercury can also have negative effects on brain function [72]. Thus, in a cross-sectional study of 129 men and women living in six villages on the Cuiaba River in Brazil, elevations in hair mercury concentrations were associated with reductions in motor speed, manual dexterity, and concentration [73]. Some aspects of verbal learning and memory were also impaired. The magnitude of these effects increased with increasing concentrations of mercury in hair. The brain functions disrupted in adults by methylmercury – attention span, fine-motor function, and verbal memory – are similar to those previously reported in children with prenatal exposures but appear to occur at substantially higher levels of exposure.

Elevated concentrations of methylmercury in blood and tissue samples are associated with increased risk for acute coronary events, coronary heart disease, and cardiovascular disease [74]. The US National Research Council concluded in 2000 that methylmercury accumulation in the heart leads to blood pressure alterations and abnormal cardiac function [75].

Subsequent research has strengthened these findings. An expert panel convened by the US Environmental Protection Agency in 2011 concluded that methylmercury is directly linked to acute myocardial infarction and to increases in cardiovascular risk factors such as oxidative stress, atherosclerosis, decreased heart rate variability, and to a certain degree, hypertension [76]. Likewise, a 2017 systematic review found that methylmercury enhances production of free radicals resulting in a long-lasting range of effects on cardiac parasympathetic activity that increase risk for hypertension, myocardial infarction, and death [77]. Further research has confirmed these findings [78,79].

Efforts have begun to estimate the contribution of mercury pollution of the oceans to the global burden of disease (GBD). A recent estimate finds that between 317,000 and 637,000 babies are born in the United States each year with losses of cognitive function that are the consequence of prenatal exposures to methylmercury resulting from consumption of mercury-contaminated fish by their mothers during pregnancy. These losses range in magnitude from 0.2 to 5.13 IQ points depending on the severity of exposure. These authors found additionally that population-wide downward shifts in IQ caused by widespread exposure to methylmercury are associated with excess cases of mental retardation (IQ below 70), amounting to 3.2% (range: 0.2–5.4%) of all cases of mental retardation in the United States [80].

The alterations of carbonate chemistry in the seas – i.e. decrease in pH, decrease in [CO₃^2–] and increase in [HCO₃^–]) – that are the consequences of increasing CO₂ absorption induce changes in the speciation of metals that alter their solubility and bioavailability and therefore their toxicity [48,81].

For example, by 2100, the projected pH of the oceans will be approximately 7.7, resulting in a 115% increase in the mean free ionic form of copper (Cu²⁺) in certain estuaries [82]. Consequently, the biotoxicity of copper to invertebrates [83] and to plankton photosynthesis and productivity will be enhanced. At the same time, however, ocean acidification will increase the concentration of dissolved iron, which could partially alleviate the inhibitory effect of copper on photosynthesis [84]. Ocean acidification appears in some instances to mitigate [85] or even reduce [86] the toxicity of mercury. As metals may play a role in the biodegradation of organic pollutants, changes in metal speciation could slow these processes and therefore potentiate the toxicity of some organic pollutants [87].

Evidence has shown that two actions will be key to preventing further addition of mercury to the oceans. These are a cessation of coal combustion and reduction of mercury use in artisanal and small-scale gold mining (ASGM). Cessation of coal combustion will not only slow the pace of climate change and reduce particulate air pollution, but will also greatly reduce atmospheric emissions of mercury and thus reduce additional deposition of mercury into the oceans. ASGM is a major source of mercury pollution of the oceans in the Global South. Actions underway under the aegis of the Minamata Convention are seeking to identify and control major sources of mercury pollution from ASGM [34].

The United Nations Joint Group of Experts on the Scientific Aspects of Marine Pollution (GESAMP) [101] estimates that land-based sources account for up to 80% of the world’s marine pollution with 60–95% of this waste comprised plastic debris.

Rivers are a major source of plastic waste in the oceans, and riverine input is estimated to be between 1.15 and 2.41 metric tons per year, corresponding to between 9 and 50% of all plastic transported to the oceans. Rivers draining densely populated, rapidly developing coastal regions with weak waste collection systems are particularly important sources [102], and it is estimated that between 88–95% of marine plastic comes from only 10 rivers [103]. Largest inputs, accounting for approximately 86% of the plastic waste entering the marine environment, are from the coasts of Asia, mainly China [89,104]. Additional sources include aquaculture, fishing and shipping [27].

Plastic wastes are gathered by oceanic currents and collect in five large, mid-ocean gyres located in the North Pacific, South Pacific, North Atlantic, South Atlantic, and Indian Oceans. The North Pacific gyre is a relatively stationary area twice the size of France that has waste from across the North Pacific Ocean, including material from the coastal waters of North America and from Japan.

Weathering, mechanical abrasion, and photodegradation break plastic waste in the oceans down into smaller particles termed microplastics (<5 mm in diameter) and still smaller particles termed nanoplastics (<1μm in diameter; defined as <100 nm by some authors) [105,106,107]. The size distribution of ocean microplastics is highly skewed, with increasing numbers of particles at smaller particle sizes [108,109]. Microplastic particles can sink downward through the water column and accumulate on the ocean floor. In contrast to microplastics, which have been measured widely in the marine environment (e.g., Text Box 1) and in marine organisms, concentrations of nanoplastics are poorly defined [110,111,112,113,114,115].

Microplastics are also manufactured. They are produced in the form of microplastic beads – polystyrene spheres 0.5 to 500 μm in diameter. These beads are used in industrial processes such as 3D printing. They also have multiple applications in human and veterinary medical products to enhance drug delivery to tissues, and in cosmetics such as toothpaste, abrasive scrubbers and sunscreen. Manufactured microplastic beads are released to the environment from these products. They enter the oceans by way of urban runoff, sewage discharge, and direct wash-off of cosmetics and sunscreens from the skin of swimmers and surfers.

Microplastics degrade in the marine environment at varying rates depending on the core material and weathering conditions. Some petroleum-based plastics can take hundreds of years to degrade, although under some circumstances photochemical degradation can be significant [97,116,117].

Microplastic particles contain substantial quantities of toxic chemicals. Toxic chemical additives are incorporated into plastics during their manufacture to convey specific properties such as flexibility, UV protection, water repellence, or color [118,119,120,121,122]. These additives can comprise as much as 60% of the total weight of plastic products. They include plasticizers such as phthalates, brominated flame retardants, antioxidants, UV stabilizers, and pigments [106,123]. Due to their large surface-to-volume ratio, microplastic particles can also adsorb toxic chemical pollutants from the marine environment – polycyclic aromatic hydrocarbons (PAHs), PCBs, DDT, and toxic metals [106].

Some plastic additives such as synthetic dyes, are classified as mutagens and carcinogens [124,125,126]. Others such as bisphenol A and phthalates are endocrine disruptors – chemicals that can mimic, block, or alter the actions of normal hormones. Perfluorinated additives, widely used in plastic to make them water-repellent, are deleterious to human reproduction. Still other plastic additives can reduce male fertility and damage the developing human brain [127,128]. Also of concern are residual unreacted monomers and toxic chemical catalysts that may be trapped in plastic during its manufacture.

Chemical additives and adsorbed chemicals can leach out of microplastic and nanoplastic particles. They can enter the tissues of marine organisms that ingest these particles, including species consumed by humans as seafood. Concentrations of some chemical additives have been found to be orders of magnitude higher in microplastic particles than in surrounding seawater [129].

Microfibers and tire-wear particles are distinct sub-categories of microplastics. Microfibers originate mainly from the clothing and textile industries [130,131,132]. Tire-wear particles are formed by the abrasion of car and truck tires. These materials reach surface waters and ultimately the oceans through runoff from roadways [133,134,135].

Plastic microfibers are distributed globally in both water and air [129,136,137,138]. They have become ubiquitous in all ecosystems. They are found in seafood [139,140]. Humans can be exposed to microfibers through consumption of contaminated fish or shellfish. Inhalation of airborne microfibers may represent an even greater source of human exposure [141,142].

Elucidation of the toxicological impacts of microplastics, including microfibers, is challenging because of their heterogeneity and great complexity [106]. Microplastics span a wide range of sizes and shapes, they are comprised of various polymer materials, and as noted above they contain myriad chemical additives, the identity of which may be proprietary and therefore not generally known. Once in the marine environment, plastics undergo weathering and adsorb additional contaminants, further enhancing their complexity. Finally, marine species exhibit a range of sensitivity to microplastics [143]. All of these factors complicate assessments of toxicity and health hazard [144,145].

Although there is evidence for transfer of additives and adsorbed chemicals from plastics to organisms, the relative contribution of plastics to total chemical exposure by all pathways is thought in most situations to be minor [146,147,148,149,150,151,152]. Likewise, although some additives and sorbed contaminants are able to bioaccumulate and biomagnify in aquatic food webs, there is not yet strong evidence that plastic particles themselves are able to undergo biomagnification [153].

Microplastics have potential to harm living organisms through several mechanisms:

The challenges associated with assessing the impacts of microplastics on marine organisms are evident in the divergent results of studies reported to date. A recent meta-analysis and review of published research on the effects of microplastics and macroplastics found similar numbers of positive and negative results [174]. A major conclusion from this and other reviews is that most of the experimental work to date has been done using concentrations of microplastics that are not environmentally relevant [144,174,175]. Future research should be conducted under more environmentally relevant conditions [174].

An additional hazard of microplastic particles and fibers in the marine environment is that they can transport and shelter hazardous microorganisms, including vectors for human disease [176]. Pathogenic bacteria have been detected on sub-surface microplastics comprised of polyethylene fibers, in plastic-containing sea surface films, and in polypropylene fragments sampled in a coastal area of the Baltic Sea [177]. Similarly, E. coli and other potentially pathogenic species have been found on plastics in coastal waters [178] and on public beaches [179]. Algal species involved in HABs [180] and ciliates implicated in coral diseases [181] have also been found attached to marine microplastics.

These findings suggest that harmful microbes and algae that colonize plastics in the marine environment may use microplastic particles to expand their geographical range (‘hitch-hiking’). Adhesion to marine plastic may also enable pathogens to increase their anti-microbial resistance thus facilitating their spread to new areas where they may cause disease and death in previously unexposed populations [177].

Consumption of contaminated fish and shellfish is a major route of human exposure to marine microplastics and their chemical contaminants [140,184,185]. Microplastic and nanoplastic particles are ingested by filter-feeders such as oysters and mussels that are then consumed by humans. Microplastic particles are found also in finfish that have consumed smaller organisms below them in the food web whose tissues are contaminated by microplastics and nanoplastics [123]. Greatest risks of human exposure are associated with consumption of small fish such as sardines that are eaten whole, including the gut [186]. The risk of microplastic ingestion may be especially great in fishing communities and in indigenous populations who rely heavily on seafood and marine mammals for their diet.

A recent study based on assessment of commonly consumed food items estimates that an average person consumes between 74,000 and 121,000 microplastic particles per year [161]. Particle consumption varies by age, sex and diet. Microplastic particles have been detected in human stool samples with about 20 particles detected per 10g of stool, indicating that these particles can reach the human gut [187]. Ingestion of contaminated drinking water and inhalation of airborne microplastic fibers are additional sources of human exposure, and inhalation may be an especially important source [138,141].

The risks that marine microplastics may pose to human health are not yet well understood and uncertainty about their potential hazard is high [125,186,188,189]. A recent review by SAPEA, an arm of the European Academies of Science, concluded that at present there is “no evidence of widespread risk to human health” of marine plastic pollution [124]. This report goes on to state, however, that as disposal of plastic waste into the oceans continues to increase and more knowledge becomes available, the assessment could change [125,126,128].

Protection of human health against the potential hazards of marine plastic requires a precautionary approach. While current knowledge of health hazards is incomplete, there is sufficient information to justify urgent action to prevent the continuing discharge of plastic waste into the oceans [190,191].

The oceans are the ultimate sink for chemical pollutants, and persistent pollutants that enter the seas from land-based sources will stay in the oceans for years and even centuries [201].

Concentrations of contaminants vary in different parts of the oceans. Therefore, tracking the levels, fate and geographic distribution of chemical pollutants is a fundamental prerequisite to predicting patterns of exposure, evaluating health effects, and designing evidence-based strategies for pollution control and disease prevention.

With the exception of crude oil, almost all of the chemical contaminants considered in this report originate on land and are transported to the ocean through atmospheric transport, river deposition, runoff, and direct discharges to the seas. In the oceans, pollutant concentrations are influenced by proximity to source, global transport patterns, and marine ecology. Highest concentrations tend to occur near population centers, industrial areas, and centers of industrialized agriculture such as concentrated animal feeding operation (CAFOs). Large-scale changes in ocean temperature and circulation induced by global climate change appear to be important drivers of pollutant distribution [202].

Atmospheric transport is a major factor governing the movement of certain manufactured chemicals from land-based sources to the sea [203]. For example, several classes of persistent organohalogen compounds, such as PCBs and fluorinated compounds volatilize at equatorial and temporal latitudes, move poleward in the atmosphere, and then precipitate to land and in water in the cool air of the polar regions, a phenomenon termed “atmospheric distillation” [204,205]. The consequences are high concentrations of persistent pollutants in marine microorganisms in the circumpolar regions as well as in top predator fish species and marine mammals. Indigenous peoples in the far north who rely heavily on marine species for food are therefore placed at high risk of exposure to POPs.

Direct dumping of industrial wastes into the sea is another source of pollution by toxic chemicals. For example, an estimated 336,000–504,000 barrels of acid sludge waste generated in the production of DDT have been dumped into the Southern California Bight [206]. The disposal process was sloppy and the contents of the barrels readily leaked leading to localized contamination. Once they are in the seas, chemical wastes can be further mobilized through natural or human-caused disturbances. For example, PCBs [207] in the Southern California Bight [206] have been mobilized by dredging of contaminated sediments from San Diego Bay.

Leaching from plastic waste is another route by which toxic chemical pollutants can enter the seas. As was described in the preceding section of this report, a wide range of toxic chemicals can leach out of the 10 million tons of plastic waste deposited in the oceans each year. These manufactured chemicals can enter the marine food chain, thus potentially resulting in ecosystem effects and human exposure.

Global efforts to reduce or eliminate pollution have resulted in some successes in control of ocean pollution, for example in reductions in PCBs and mercury in the seas surrounding Europe (EEA) [27,208]. In general, however, halogenated organic compounds, such as those governed by the Stockholm Convention, are highly resistant to degradation in the marine environment, and these persistent legacy pollutants remain widespread in marine environments.

An estimated 1–3 billion people depend on seafood as their principal source of dietary protein. Thus, contaminated seafood is the major route of human exposure to marine pollutants. The chemical pollutants most often identified in seafood are methylmercury, PCBs, dioxins, brominated flame retardants, perfluorinated substances, and pesticides.

Factors that influence concentrations of chemical pollutants in fish include geographic origin, fish age, fish size, and species. Geographic origin is a highly important determinant of pollutant load [209,210,211] and often outweighs the influence of other factors (Figure 7). Thus, fish that live and are caught near cities and major points of pollutant discharge typically contain highly elevated concentrations of POPs and other chemicals [193].

Predator fish species at the top of the food web generally accumulate higher concentrations of chemical pollutants than fish at lower trophic levels. Therefore, fish consumption advisories typically focus on limiting consumption of predator species. However, given the vast scale of the oceans and wide geographic variation in pollutant concentrations, it is perhaps not surprising that that these advisories do not always adequately protect consumers. For instance, one survey found that sardines, a species relatively low on the marine food web, can have higher concentrations of PCBs than cod or salmon [212].

Toxic chemical pollutants in the oceans have been shown capable of causing a wide range of diseases in humans. Toxicological and epidemiological studies document that toxic metals, POPs, dioxins [213], plastics chemicals, and pesticides can cause cardiovascular effects, developmental and neurobehavioral disorders, metabolic disease, endocrine disruption, and cancer (detailed references are provided in the following paragraphs). Effects in humans and laboratory animals are generally similar. Independent, systematic reviews undertaken by the US National Academy of Medicine and the International Agency for Research on Cancer confirm and validate these findings [214,215].

Appendix Table 1 in the Supplementary Appendix to this report summarizes the known links between exposures to toxic chemicals in the oceans and a range of human health outcomes. Key associations are the following:

More than 10,000 chemicals are used in the manufacture of pharmaceuticals and personal care products (PPCPs). These products include therapeutic drugs with both medical and veterinary applications, cosmetics, and cleaning products. They are a subset of the manufactured chemicals discussed in the preceding section. Like pesticides, pharmaceuticals are specifically designed to have biological effects, and thus even low-dose exposures can affect living organisms, including humans.

With increasing manufacture and use of pharmaceuticals by a growing global population, pharmaceutical wastes have entered ecosystems in increasing quantities. Pharmaceutical and cosmetic manufacturing plants, hospitals, nursing homes, confined animal feeding operations (CAFOs), and aquaculture can all release PPCPs into wastewater systems, rivers, and eventually the oceans. Environmentally persistent pharmaceutical pollutants (EPPPs) have been recognized as a “new and emerging issue” under the United Nations’ Strategic Approach to the International Management of Chemicals (SAICM) since 2015.

Therapeutic drugs commonly found in measurable quantities in urban wastewater and coastal waters include ibuprofen and other painkillers, anti-depressants, steroids, caffeine, estrogens and other hormone-containing products, anti-epileptics, cancer drugs, antimicrobials such as triclosan, and antibiotics [274,275,276,277]. Many pharmaceutical and cosmetic products in current use contain manufactured plastic nanoparticles [278].

Some PPCPs have potential to accumulate in fish and shellfish species consumed by humans and thus have potential to affect human health [279]. Concern is growing that pharmaceutical chemicals and their metabolites can damage marine species through a range of toxicological mechanisms, including endocrine disruption and neurotoxicity. A recent case study suggests that the widely used sunscreen chemical, oxybenzone (benzophenone-3) may have toxic effects on the larval forms of several coral species [280]. The study reports that these effects include transformation of coral larvae from a motile state to a deformed, sessile condition; increased coral bleaching; leading to deformed skeleton formation; and DNA lesions.

Manufactured chemicals are rarely present in the environment in isolation, but instead are found in complex mixtures. This complicates assessment of health impacts, because toxicological tests most often are conducted on one chemical at a time, thus potentially missing additive, antagonistic, or synergistic actions that could result from simultaneous exposures to mixtures of POPs and other manufactured chemicals that occur together in the oceans as “chemical cocktails” [281,282]. Future public health studies should pay additional attention to complex mixtures and cumulative risk assessment. The possibility of interaction among multiple POPs raises the question as to whether any one chemical that shows an association with disease is really acting a “proxy” for the combined effect of all the chemicals [283,284].

Consideration of the susceptibility of exposed populations is also important. The safe limit for exposure at sensitive life stages of development, in utero or in nursing infants, will be lower than for adults. And in the adult population, underlying disease may modify risk. Finally, “safe” levels for one pollutant may not pertain to the combined risk from simultaneous exposure to the many pollutants to which a person may be exposed.

Because of widespread pollution of the oceans by toxic metals and POPs and contamination by HAB toxins (discussed in the next section of this report), it is necessary to balance the risks of chemical pollutants in seafood against the benefits derived from nutrients unique to fish and shellfish. Thus, the benefits of essential fatty acids (EPA and DHA) in farmed and wild fish must be balanced against the risks for adverse health outcomes from chemical contaminants in those same fish [285,286].

To assess whether the beneficial effects of omega-3 fatty acids in seafood may mitigate the adverse effects of methylmercury on brain development, IQ was measured in 282 school-age Inuit children in Arctic Québec whose umbilical cord blood samples had been analysed for mercury and DHA [287,288]. The investigators found that prenatal mercury exposure was associated with lower IQ after adjustment for potential confounding variables. Incorporation of DHA into the model significantly strengthened the association with mercury, supporting the hypothesis that the beneficial effects of DHA intake can at least partially offset the harmful effects of mercury [65].

Similarly, some studies have noted that the beneficial effect of fish consumption on the cardiovascular system appears to be reduced by co-exposure to PCBs [289]. The risk differential between wild and farmed salmon is a prime example of these concerns. While the abundance of omega-3 as well as omega-6 fatty acids differ between wild and farmed fish, both contain high levels of these beneficial compounds. However, farmed fish tend to have higher levels of PCBs and other contaminants than wild fish, and contaminant burdens differ between fish farmed in different parts of world. Determining risk of those contaminants depends in part on which outcome is considered, and whether the risk is from one or many chemicals.

Studies comparing relative risk of cancer and other health outcomes associated with dioxin-like compounds in salmon concluded that consumption of farmed salmon would need to be limited to many fewer meals per month than for wild salmon, to reduce cancer risk to a level near the WHO “tolerable daily intake” for dioxin-like compounds [290,291].

A review examining the health risks and benefits of seafood consumption and the impact of fish consumption on sustainability of fish stocks concluded that “few, if any, fish consumption patterns optimize all domains”, but called for development of “comprehensive advice … to describe the multiple impacts of fish consumption” [292]. Several groups have disseminated such guidance [293,294,295].

HABs are not a new phenomenon and some occur naturally. However, the frequency and magnitude of HAB events appears to be increasing [328]. These increases have been linked to three factors:

Increases in frequency and severity of HAB events have been linked to increasing coastal pollution in the Seto Inland Sea of Japan in the mid-1970s [332] and in the northwestern Black Sea in the 1970s and 1980s [333]. Both of these situations have subsequently been remediated, and case studies describing these and other successful remediation efforts are presented in the section of this report on Successes in Prevention and Control of Ocean Pollution [334].

A current example of the effect of increasing coastal pollution on HAB frequency is seen at the mouth of the Changjiang River in China, where nitrate concentrations have increased four-fold in the past 40 years and phosphate concentrations have increased by 30%. The main drivers are increases in population size and agricultural production. Significant increases in algal biomass and a change in the composition of the phytoplankton community have resulted. The frequency of local HABs has increased dramatically [335].

Increases in the frequency and severity of HABs have been linked to changing weather patterns such as major warming events, increased runoff, and changes in ocean currents (Figure 10). Examples include recent Alexandrium blooms in the northeastern United States [336] and massive blooms of Pseudonitzschia on the US west coast associated with a mesoscale warm-water anomaly termed “the blob” [337]. These events presage projected future climate scenarios [54,338,339].

Sea surface warming leads to range extensions of HAB species and to the appearance of algal toxins in previously unaffected areas [53,55,340,341,342,342]. An example is seen in the recent, first ever detection of HAB toxins in Arctic waters [343]. The movement of harmful algae into the Arctic coupled with northern indigenous peoples’ lack of experience with HAB toxins put these populations at high risk of exposure and disease. This risk is compounded by lack of knowledge about uptake of HAB toxins by species such as whales, walruses, seals, and seabirds used by northern indigenous people as food sources.

Another example of climate-driven change in HAB range that has already occurred is poleward extension in the geographic ranges of the benthic dinoflagellates responsible for ciguatera poisoning into warm-temperate habitats, for example from the Caribbean Sea northward into the Gulf of Mexico [55,342,344]. This range extension appears to be associated with warming sea surface temperatures and higher storm frequencies, and destruction of coral reefs [345,346,347,348,349]. It is reflected in increased numbers of calls about ciguatera poisoning to poison control centers in the United States.

An impact on HAB biology that appears to reflect synergy between global climate change and ocean acidification is the observation that HAB toxins can become more potent at higher temperatures or under more acidic conditions [350,351]. This change may reflect temperature-induced shifts in the relative abundance of dinoflagellate species [340,352,353].

Consumption of fish and shellfish that have ingested toxic algae is a major route of human exposure to HAB toxins. Filter-feeding shellfish such as oysters and mussels pose an especially high risk because these species ingest toxic algae and then accumulate algal toxins to high concentrations that can cause acute disease and sudden death in shellfish eaters. The poisoning syndromes caused by HABs in shellfish include paralytic, neurotoxic, amnesic, diarrhetic, and other gastrointestinal poisoning [354,355]. Consumption of finfish and shellfish containing ciguatera toxin may also result in ciguatera poisoning.

Human exposure to HAB toxins can also occur through skin or respiratory contact via swimming or visiting beaches during algal blooms. People have reported skin rashes, respiratory irritation such as sneezing, and a burning or itching in the nose or throat while swimming, visiting, or working at the beach during Karenia brevis red tide events [356,357]. People with asthma appear to be at particular risk [358]. Karenia brevis blooms are associated additionally with increases in emergency room admissions for respiratory, gastrointestinal, and neurologic illnesses [359,360,361]. There is evidence that people experience adverse effects also during Sargassum blooms [362] and from exposures to algal-derived palytoxins [363].

Macroalgal blooms, can harm human health by causing massive accumulations of algae in bays and on beaches. When these piles of algae decompose, they can release foul-smelling and hazardous gases, including hydrogen sulfide, methyl mercaptans, and dimethyl sulfide [364]. Coastal populations exposed to decomposing algal mats have reported eye and respiratory tract irritation.

HABs cause a variety of human diseases, some of them extremely serious (Text Box 3). HAB-related illnesses are for the most part acute, and acute reference doses (ARfD) have been derived to protect the public against these acute exposure events (See Appendix Table 2 in the Supplementary Appendix). Little research has been done to evaluate chronic illness after either acute or chronic exposures to HAB toxins, and information on long-term health effects is still insufficient to allow determination of tolerable long-term daily intakes (EFSA opinions or FAO/WHO/IOC ad hoc expert consultation).

Children may be more likely than adults to be affected by HAB toxins due to a combination of greater exposure, riskier behaviors, and sensitive developmental stage. Children also consume more food per unit body weight than do adults and thus may receive higher relative doses [365].

The frequency and severity of some HAB events can be controlled by reducing releases of nitrogen, phosphorus, animal wastes, and human sewage into coastal waters. (See Text Boxes 9–13). Additional actions that can be taken to mitigate HABs are the following:

Routine monitoring for HAB toxins in shellfish is key to the prevention of human illness caused by these toxins. Monitoring programs are typically embedded within comprehensive shellfish safety programs. Details are presented in the Monitoring of Ocean Pollution section of this report.

Another strategy for mitigating the impact of HAB toxins on human health is to process harvested shellfish in such a way as to reduce toxicity to an acceptable level. An example is the removal of scallop viscera and marketing of only the adductor muscle, which generally contains little or no HAB toxins [389].

HABs have multiple negative economic and social effects. In the US, it is conservatively estimated that the average annual cost of marine HABs is USD $95million [392]. Health impacts are responsible for the largest component of these economic loses [331]. Economic losses attributable to HABs are estimated to $850 million (USD) annually in Europe and over $1 billion (USD) in Asia [392]. The costs of individual catastrophic HAB events can be overwhelming. Mexico, for example, spent $17 million in 2018 to remove 500,000 tons of Sargassum from its Caribbean beaches and declared a state of emergency. Another large HAB resulted in the largest fish farm mortality ever recorded and a loss of USD $800 million [339]. Increased frequency of respiratory ailments, aerosolized toxins, noxious gas, dead fish, proliferation of biting sand fleas from decaying piles of macroalgae, and discolored waters drive tourists away from beaches, change recreational habits, and thus reduce income from tourism in coastal communities [393,394,395,396].

Marine bacteria of the genus Vibrio are particularly important causes of disease and death [403]. Vibrio cholerae, the causative agent of cholera, is the species of greatest concern. Vibrio species exhibit strong seasonality, and warmer water temperatures result in increased concentrations in estuarine and coastal waters [50,51,404,405,406,407,408]. Further warming of coastal waters caused by climate change is likely to further increase abundance of Vibrio bacteria and expand their geographic range [409]. These changes will likely result in increased frequency of Vibrio infections in coming decades and possibly to appearance of Vibrio infections in previously unaffected areas [52]. There is some indication that after extreme weather events such as hurricanes, droughts, and tropical storms shifts occur in the composition of Vibrio species and that these shifts are driven by discharges of sewage and inorganic nutrients into coastal waters [410].

Vibrio parahaemolyticus and Vibrio vulnificus are two additional Vibrio species that pose grave risks to human health [412,413]. These organisms are now appearing for the first time in previously cold waters at northern latitudes with major peaks occurring during warm summers (Figure 11) [411]. This trend is particularly well documented for the Baltic Sea, where the annual incidence of Vibrio infections is reported to almost double for every one-degree increase in sea surface temperature (Figure 12) [402,414]. Similar trends have been reported in the United States where incidence of infections by Vibrio species has increased by 115% in the past decade, especially along the Gulf, Northeast, and Pacific Northwest coasts [50,414,415].

Vibrio vulnificus can enter the human body either through ingestion of contaminated seafood or through open wounds [417]. When V. vulnificus, known colloquially as ‘flesh-eating bacteria’, enters an open wound it can cause severe infections such as necrotizing fasciitis (Text Box 5).

Ingestion of shellfish contaminated by V. vulnificus, especially oysters, causes more than 90% of cases of V. vulnificus gastroenteritis [418,419]. This reflects the fact that filter-feeding shellfish such as oysters, clams, and mussels can concentrate Vibrio by several orders of magnitude over concentrations in seawater [412,418].

Vibrio vulnificus gastroenteritis can progress very rapidly to septicemia – sometimes within 24 hours after ingestion of contaminated seafood [418,420]. Even with aggressive medical treatment, the case-fatality ratio for Vibrio vulnificus septicemia is greater than 50%. Vibrio vulnificus thus has the unlovely distinction of having the highest case-fatality ratio of any foodborne pathogen [418,420]. It is the cause of 95% of seafood-borne deaths in the USA [420].

Recent data suggest that rising sea surface temperature may expand not only the temporal and spatial distribution of Vibrio species, but also increase the virulence and antimicrobial resistance of some Vibrio strains [421,422,423].

Salinity is another factor that affects the abundance of Vibrio species in marine environments. Typically, V. vulnificus and V. parahaemolyticus are not prevalent in waters where salinity exceeds 25 parts per thousand. Recent anecdotal reports from the UK, EU, and Brazil indicate, however, that shifts in the composition of Vibrio communities in estuarine systems and increases in Vibrio infections are now being recorded in waters where salinity is greater than 30 parts per thousand [431], possibly reflecting an interaction between salinity and sea surface warming. A decade-long study of Vibrio conducted in the Neuse River Estuary in North Carolina, USA, has shown the temperature is not increasing in that system, and that temperature increase cannot therefore explain the significant increase observed in Vibrio concentrations (Figure 13) [424].

In some major river basins (i.e., the Amazon, the Ganges, the Brahmaputra, and the Congo), increased incidence of Vibrio infection is reported to coincide with high sea surface temperatures and high discharge events, events that typically are associated with abnormal phytoplankton growth [432]. In other marine coastal areas, the global abundance of Vibrio has been shown to correlate with chlorophyll, acidity, maximum sea surface temperature, and salinity [50].

Allochthonous bacteria are microorganisms not native to marine environments that are introduced into coastal waters from land-based sources. Allochthonous pathogens of greatest concern include virulent Enterococcus species, Escherichia coli serotypes (e.g., O157:H7), Campylobacter species, Clostridium species, Shigella species, and Salmonella species [433].

Pathogenic bacteria can enter coastal waters through sewage effluent, agriculture and storm water runoff and wastewater discharges from ships [434]. Rivers, especially those near major population centers, are an important source [434]. Through horizontal gene transfer, allochthonous bacteria can introduce harmful new genetic traits into indigenous marine microorganisms thus increasing their virulence and their capacity for anti-microbial resistance [435].

Climate change is accelerating the introduction, dispersion, and growth of allochthonous bacteria in coastal waters. For example, rising sea surface temperatures have been shown to increase the abundance of Salmonella species in Hawaiian coastal streams [436]. Warming may also increase the variability of salinity gradients along coastlines [437] thus affecting the growth and persistence of fecal-oral pathogens and increasing risk for major outbreaks of diarrheal disease [438].

Fecal-derived bacteria in marine environments tend to bind to particle surfaces (sediment, sand, plastics) where they form biofilms that enhance their survival. In estuarine environments, for example, the concentration of fecal bacteria is generally one or more orders of magnitude higher in surface sediments (per 100 g dry weight) than in the water column (100 ml). The survival of fecal bacteria in the oceans is thus positively linked to concentrations of pollutants and other suspended matter in the water column [439,440,441].

Bacterial pathogens in the marine environment are responsible for a wide range of acute and chronic diseases. These include diarrhea and gastroenteritis, ocular and respiratory infections, hepatitis, and wound infection. Transmission of disease occurs mainly through ingestion of contaminated water and consumption of contaminated seafood [433].

From 1973 to 2006, 188 outbreaks of seafood-associated infections causing 4,020 illnesses were reported to the Foodborne Disease Outbreak Surveillance System in the United States [442]. Most of these outbreaks were due to bacterial agents (76.1%), a significant proportion of them linked to pathogens with a human reservoir such as Salmonella and Shigella [443,444] (Table 2).

Antimicrobial resistance (AMR) is likely to have been present for millions or billions of years in marine microbial communities as the result of resistance mechanisms that bacteria have evolved in response to naturally occurring threats [446].

More recently, however, the prevalence of AMR has been increasing in marine environments, especially in coastal waters. These increases appear to reflect increasing introductions from land-based sources of allochthonous bacteria that carry resistance genes that can be passed to marine bacteria through horizontal gene transfer [16,447]. Such exchanges may account for the acquisition of AMR by indigenous pathogens such as Vibrio.

The development of confined animal feeding operations (CAFOs) to enhance livestock production and increase the profits in the poultry, beef, and swine industries have further promoted the development of AMR bacteria. These facilities are associated with poor waste treatment practices, and the vast quantities of effluent they release into waterways and directly into the ocean are associated with increased genetic encounters across “promiscuous” bacterial species able to transfer resistance genes horizontally.

An increasing body of evidence documents that significant human exposure to AMR bacteria can occur in coastal environments. A study in the UK reports that an estimated 6 million exposures occur per year to cefotaxime-resistant E. coli [448]. Another study found an increased probability of gut colonization by cefotaxime-resistant E. coli, a known risk factor for infection, in persons such as swimmers and surfers heavily exposed to contaminated recreational waters [449]. Recent studies of near-bottom waters from the Polish coastal zone reported multiple antibiotics at ng/L concentrations, with enrofloxacin reported at >200 ng/L [450,451].

Viruses in coastal and estuarine systems that pose serious threats to human health include the Picornaviridae (enteroviruses, e.g., poliovirus, coxsackievirus, and echovirus), Adenoviridae (adenovirus), Astroviridae (astrovirus), Reoviridae (reovirus, rotavirus) and most significantly the Caliciviridae, a genus that includes norovirus and calicivirus [452]. Norovirus infections represented 21% of enteric virus infections reported from recreational water exposures across the USA from 2000–2014 [453]. Noroviruses enter coastal waters through stormwater, flooding, illicit boat discharges, and sewage system leaks and spills (E.g., Text Box 6).

Dramatic improvements have been made in the past decade in diagnostic technologies for direct quantification of viral pathogens in marine environmental samples. These include new molecular approaches such as digital droplet PCR [454].

Parasitic infections associated of marine origin are increasing in number and geographic range in response to climate change [456]. Cryptosporidiosis, giardiasis, and salt water schistosomiasis are the most common of these infections [453,457,458,459].

Two emerging human parasitic diseases of particular concern in the ocean environment are Anisakiasis (a zoonosis caused by the fish parasitic nematode, Anisakis) and Diphyllobothriasis (caused by the adult tapeworm, Diphyllobothrium nihonkaiense) [460]:

Monitoring of chemical and plastic pollution in the oceans has been ongoing for decades. One approach has been direct measurement of discharges of pollutants such as waste plastics into the seas from land-based sources, and tabulation of the number and frequency of discharge events such as oil spills. Under the aegis of the Horizon 2020 Initiative for a Cleaner Mediterranean, the European Environment Agency, and UNEP-MAP have defined a set of indicators that will potentially enable an integrated assessment of key land-based sources of pollution in European seas, including solid waste and marine litter.

A key monitoring strategy for toxic chemical pollutants is to measure concentrations of indicator pollutants in seawater or in organisms that are “sentinel species”. Since the 1970s, the U.S., the European Environment Agency, and the International Mussel Watch Program have measured geographic patterns and temporal trends in concentrations of organic chemical and heavy metal pollutants along the coasts, through analysis of residues in bivalve mollusks [535]. These programs have identified locations where heavy metals, POPs, and pesticides are most highly abundant and have highest potential to contaminate seafood. These programs have documented that pollutant concentrations are highest near urban areas [536].

Evaluation of molecular biomarkers of exposure to chemical contaminants is an important complement to direct measurement of chemicals [531,537]. Biomarkers have been used to assess exposures and early biological effects of exposures to oil spills, PCBs, dioxins, toxic metals, and endocrine disruptors [538]. Pollutant levels in broad areas of the open ocean can be inferred by analysis of tissue levels in large ocean species that serve as biological monitors. Thus, measurement of levels of chemical pollutants and of molecular biomarkers of exposure has been done by analysis of skin biopsies of sperm whale [536]. Studies in tissues of large sharks and finfish (yellowfin tuna) provide similar data [210,539].

Future Directions in Monitoring of Chemical and Plastic Pollution in the Oceans.

Several international and European systems currently capture and disseminate information about HAB events, their predisposing factors, and HAB- related illnesses [542,543]. Other initiatives are being coordinated by the Intergovernmental Panel for Harmful Algal Blooms (UNESCO, IPHAB) collaboration. Specific initiatives are summarized in the following, Tables 3 and 4:

Serious challenges impede the detection, quantification and prediction of viral, bacterial, and parasitic pathogens in seafood, shellfish, and oceanic waters as well as in aquaculture operations. Although molecular diagnostics and other tools have improved dramatically over the past two decades [454,551], additional advances are required to better detect and quantify pathogens in water, seafood products, aquaculture facilities, and shellfish meats [552].

The significant relationships observed between pollution concentrations, rising sea surface temperatures, Vibrio infections and HABs have catalyzed the development of modeling efforts. These models incorporate multiple layers of geocoded data and are designed to generate predictive forecasts [553]. New technologies such molecular and bioinformatics-based diagnostics [410,425,554], metabarcoding, “big data” mining and machine learning may be expected to contribute to further development of these efforts [40,555,556]. Implementation of real-time PCR-based approaches has already been shown to be a useful tool for diagnosing V. vulnificus wound infections [554].

A mapping tool developed by the European Centre for Disease Prevention and Control (ECDC) [416] is now operational and is providing 24-hour updated Vibrio risk data freely available to the community. However, this system has not yet been implemented by all EU Member States. Also, it needs to be further developed to incorporate relevant variables associated to major climatic events that have been proven to have an impact.