CONTAMINATION AND POLLUTION

Pollution is caused by an exposure to chemicals or energy at an intensity that exceeds the tolerance of organisms. As such, pollution is judged to have occurred when it can be shown that organisms have suffered toxicity, or other kinds of ecological damage can be demonstrated. Pollution can affect humans and other species, as well as communities and ecoscapes. Pollution is often caused by an exposure to chemicals in large enough concentrations to poison at least some organisms. However, pollution can also be caused by non-toxic exposures, such as the excessive fertilization of a waterbody, a release of waste heat into the environment, or the discharge of raw sewage containing pathogens.

Contamination refers to those much more common situations in which potentially damaging stressors are present in the environment, but at an intensity too low to cause measureable damage. For instance, a certain chemical may occur in a higher concentration than is normally encountered in the environment. However, if its concentration is too low to cause measurable toxicity to at least some organisms, or to affect other ecological components or processes, the chemical is a contaminant rather than a pollutant.

In fact, metals such as aluminum, cadmium, lead, mercury, and zinc are present in all parts of the environment, including all organisms, in at least a trace concentration. If the detection limits of the available analytical chemistry are sensitive enough, this “universal contamination” by metals can easily be demonstrated. Although all metals (and any other chemicals) are potentially toxic, they must be present in a high enough concentration for a long enough period of time to actually poison organisms and cause ecological damage. In other words, the exposure must exceed biological tolerances before damage is caused and pollution can be said to occur.

In the modern world, an enormous amount of pollution is associated with human activities. This has caused important damage to human health and to managed and natural ecosystems. People cause pollution in diverse ways, and we examine them in following chapters. Most commonly, anthropogenic pollution is associated with these kinds of activities:

• accidental or deliberate emissions of chemicals into the environment, such as sulphur dioxide, metals, pesticides, and petroleum;
• releases of substances that react in the environment to synthesize chemicals of greater toxicity – this is known as secondary pollution (as occurs when ozone is created by photochemical reactions in the atmosphere);
• emissions of chemicals that degrade stratospheric ozone, such as chlorofluorocarbons;
• releases of waste industrial heat, as when a power plant discharges hot water into a river or lake;
• discharges of nutrient-laden sewage or fertilizer into waterbodies;
• emissions of greenhouse gases that threaten global climate; or
• releases of alien species that cause damage when they invade managed or natural habitats, or are pathogens of people, crops, or native species.

Image 15.5. Many human activities result in emissions of pollutants into the environment. This image shows a 380-m smokestack at a metal smelter near Sudbury, Ontario. Source: B. Freedman.

contaminants in the environment

All of the naturally occurring metals and other elements are ubiquitous (found everywhere) in at least trace concentrations in soil, water, air, and organisms. As long as the detection limits of the available analytical chemistry are low enough, this universal contamination can always be demonstrated.

Organisms require some of the trace elements as essential micronutrients, including copper, iron, molybdenum, zinc, and in some cases aluminum, nickel, and selenium. Under certain conditions, however, these same elements can accumulate to high concentrations in organisms and cause ecological damage (see In Detail 18.1). Trace elements that are most often associated with environmental toxicity are the heavy metals cadmium, chromium, cobalt, copper, iron, lead, mercury, nickel, silver, tin, and zinc, as well as the lighter elements aluminum, arsenic, and selenium.

Some cases of elemental pollution are natural in origin. This usually involves metal-rich minerals being exposed at the surface and causing local ecological changes. However, human activities have caused additional examples of pollution by toxic elements, particularly in the vicinity of industrial sources such as smelters. In addition, emissions of mercury and lead from power plants and automobiles have caused widespread contamination of remote environments, although it is not yet certain that this is causing ecological damage.

There are cases of people having been poisoned by exposure to toxic elements in their environment. Some historians believe that the decline of the Roman Empire may have been hastened by neurotoxicity caused by chronic lead poisoning. The Romans had significant exposure to lead because they stored acidic beverages (such as wine) in pottery treated with pigments and glazes that contained lead. As well, their water piping was made of lead (the word “plumbing” is based on the Latin word for lead – plumbum). In nineteenth-century Britain, many people who made felt top-hats developed neurological damage because of their exposure to mercury compounds used to give a shiny finish to the hats – hence Lewis Carroll’s character in Alice in Wonderland, the “Mad Hatter,” and the expression “mad as a hatter.”

More recently, thousands of people suffered mercury poisoning during the 1960s after they ate grain that had been treated with mercuric fungicide. In one disastrous case in Iraq in 1971, more than 6,500 people were poisoned (about 500 died) when they ate food prepared from mercury-treated grain. The grain had been donated by a foreign aid program and was intended only for planting. Although the sacks of grain were labelled to indicate that the seeds were poisonous, many of the victims were illiterate or did not understand or ignored the implications of the message. About the same time, similar poisonings occurred when people ate mercury-treated grain in Guatemala, Iran, and Pakistan. To avoid these problems today, fungicide-treated seed-grain is usually dyed red, which warns people not to use it as food.

Mercury also caused thousands of cases of poisoning at Minamata, Japan. A factory there had discharged elemental mercury into Minamata Bay. In that form mercury is not very poisonous, but microbes in the sediment transformed the metal into methylmercury, which is extremely toxic and bio-accumulates in organisms in preference to the water of their aquatic environment. The methylmercury further biomagnified up the food web and caused extensive poisoning of fish-eating birds, domestic cats, and people (see In Detail 18,1 and Global Focus 18.1). In this chapter, we examine natural and anthropogenic pollution with toxic elements and the resulting ecological consequences.

In Detail 18.1. Bioaccumulation and Biomagnification
Certain metals or their organic compounds, such as methylmercury, tend to occur in much higher concentrations in organisms than in the ambient, non-living environment. This phenomenon is known as bioaccumulation (also called bioconcentration). Similar tendencies are shown by chlorinated hydrocarbons, such as DDT, PCBs, and dioxins (see Chapter 21). Bioaccumulation occurs because certain substances have a strong affinity for organisms and therefore concentrate within them in preference to their non-living environment. Many of these chemicals dissolve in biological fluids and tissues, such as lipid (fat), in preference to ambient water or soil.

Another phenomenon, known as biomagnification (or food-web magnification), is the tendency for top predators to have the highest concentrations of these chemicals. Organisms are highly efficient at assimilating methylmercury and organochlorines from their food. Therefore, these chemicals become stored in organisms, rather than being excreted. This means that predators at the top of the food web develop the highest concentrations (residues) of these chemicals. Usually, bioaccumulation and food-web magnification progress with age, so the oldest individuals in any population are the most contaminated.

Figure 18.1. Biomagnification leads to progressively higher concentrations of methylmercury and chlorinated hydrocarbons in organisms higher in the food web. The common loon (Gavia immer) is a top predator in many lakes. In some regions of Canada, these birds can harbour concentrations of methylmercury that are high enough to impair their reproduction. The source of the environmental mercury is not yet known for certain, but it may be associated with anthropogenic emissions from power plants, incinerators, and smelters.

Concentration and Availability

All of the naturally occurring elements are present in at least trace concentrations in all samples of water, soil and rocks, air, and organisms. The term background concentration refers to a presence that is not significantly influenced by either anthropogenic emissions or unusual natural exposures. The background concentration in soil and rocks is usually much higher than in water, and also generally higher than in the tissues of organisms (Table 18.1).

However, elements that are dissolved in water often occur in chemical forms (such as ions) that are relatively easily absorbed by organisms. For this reason, even a trace aqueous concentration may be toxic. In contrast, the much higher concentrations that commonly occur in soil and rocks are mostly insoluble, and therefore are not particularly bioavailable. Scientists determine the total concentration of metals in a component of the environment (such as soil, sediment, or rock) by digesting a sample in a hot mixture of strong acid. In contrast, the “available” concentration is determined from an aqueous (water) extract of a sample. In general, the available concentration of toxic elements in soil are much smaller than the total concentrations (generally less than 1% of the total value), and it is also much more relevant to potential toxicity.

Most elements are found in only trace concentrations in the environment (Table 18.1). In contrast, aluminum and iron are prominent constituents of rocks and soil, with concentrations typically about 8% and 3-4%, respectively. However, almost all of the aluminum and iron in soil and rocks occurs as insoluble minerals that are not readily available for uptake by organisms. For example, virtually all aluminum in soil occurs as insoluble silicate and clay minerals. Although aluminum in these forms comprises about 8% of the soil mass, it is not available for uptake by plants and is therefore non-toxic. However, much smaller concentrations of aluminum, typically only a few parts per million (ppm), are found as ions, either bound to organic matter and clay surfaces or freely dissolved in soil water. The ionic forms of aluminum are readily available for biological uptake and may cause toxicity to species that are sensitive to this metal.

Much higher concentrations of soluble available aluminum occur in strongly acidic environments, especially when the pH is less than about 5.5. (In fact, almost all metals are much more soluble under acidic conditions.) Aluminum solubility is also greater in strongly alkaline environments, with pH higher than about 8. Moreover, different ionic species of aluminum occur at different pH levels:

• Al³⁺ is dominant in strongly acidic environments with a pH less than about 5.0
• AlOH²⁺ and Al(OH)₂+ are important under less acidic conditions of pH 4.5–5.5
• Al(OH)₃ from pH 5.2–9.0
• and AlOH₄– in alkaline environments with pH greater than 8.5.

Aluminum toxicity is a common problem for organisms that live in highly acidic or alkaline environments. This is because of the combined influences of greater solubility and the presence of relatively toxic ions under those conditions.

Table 18.1. Background Concentration of Elements in Selected Components of the Environment. Source: Data from Bowen (1979).

Toxicity

The toxicity of elements and other chemicals is related to two factors: (1) the exposure (dose) and (2) the vulnerability of an organism to the particular substance. The dose received is influenced by the available concentration in the environment and the period of exposure. Therefore, a long-term exposure to only a minute available concentration may cause toxicity, especially if the element is able to bioaccumulate and then biomagnify in the food web until it exceeds a threshold of biological tolerance.

Organisms vary greatly in their tolerance of exposures to toxic elements (and to all other poisons). Consequently, an intense exposure to a potentially toxic chemical may result in some species being poisoned, while tolerant ones may not be damaged and may even benefit from the demise of sensitive species in their community. In addition, there is usually genetically based variation for tolerance within a species. This can lead to the evolution of populations (known as ecotypes) that are relatively tolerant of toxic exposures (we examine this topic in the next section).

The most common mechanism of poisoning by toxic elements is damage to an enzyme system. (Organisms have a huge diversity of enzymes, which are proteins that catalyze specific biochemical reactions and are critical to healthy metabolism.) The poisoning occurs because metal ions bind to specific enzymes, which changes their shape and results in a loss of their unique catalytic function. Toxic elements may also cause poisoning by binding to DNA or RNA, thereby disrupting transcription and translation, the processes by which genetic information is used to produce specific proteins (including enzymes; see In Detail 6.1). Toxic metals can also disrupt DNA replication and hence cell division.

Typical symptoms of acute poisoning caused by toxic elements in plants include abnormal patterns of growth, decreased productivity, impaired reproduction, the occurrence of disease, and ultimately death. Symptoms of chronic toxicity are harder to detect and may include a “hidden injury” such as a decrease in productivity that occurs without signs of acute damage. Animals can show a variety of symptoms associated with enzyme disruption, often including neurotoxicity and impaired functioning of the kidneys, liver, and other organs.

Ecotoxicology

Toxicology is the science of the study of poisons. It examines their chemical nature and effects on the physiology of organisms. If the dose (exposure) is large enough, any chemical, even water, can cause toxicity.

Environmental toxicology is a broader field than conventional toxicology. In addition to studying the biology of poisoning, it also examines environmental factors that influence the exposure of organisms to potentially toxic chemicals. Important topics in environmental toxicology are the following:

• the cycling and transportation of potentially toxic chemicals
• their transformation into other substances (which may be more, or less, poisonous than their precursors)
• the determination of sinks where chemicals may accumulate in especially high concentrations, including within the bodies of organisms

Ecotoxicology has an even broader domain because it studies the direct poisonous influences of chemicals as well as indirect ones. Examples of indirect ecological influences include changes in habitat or in the abundance of food. For instance, the use of a herbicide in forestry or agriculture will affect the biomass and species composition of the vegetation on a treated area. These are important changes in the habitats of animals. Even if the herbicide does not poison animals that are exposed to the spray, they may be affected by changes in their habitat. A complex of factors influences the ecotoxicological risks associated with exposure to chemicals in the environment. The most important factors are:

1. biological sensitivity,
2. the inherent toxicity of the chemical being considered,
3. the intensity of the exposure, and
4. any indirect effects that might be caused.

These considerations are examined below.

In Detail 15.1. What Is Toxicity? In the biological sense, a chemical can poison an organism if it detrimentally affects some aspect of its metabolism. This effect is called toxicity. A toxic chemical may, for example, disrupt the functioning of an enzyme system or interfere with cellular division. However, the legal definition of toxic substance, as stated by the Canadian Environmental Protection Act, is as follows: “A substance is defined as toxic if it enters or may enter the environment in a quantity or concentration or under conditions that: (1) have or may have an immediate or long-term harmful effect on the environment; (2) constitute or may constitute a danger to the environment on which human life depends; or (3) constitute or may constitute a danger in Canada to human life or health.”

This definition has legal standing in Canada, and it is used in the management and regulation of a wide variety of chemicals.

However, this definition is inadequate in some important respects, particularly because it deals only with extremely toxic chemicals, under conditions in which they occur in high concentrations. Substances whose acute toxicity is less may cause subtle, long-term damage to people, other species, and important ecological values. These kinds of exposures are not dealt with by this definition.

 

1. Biological Sensitivity

Sensitivity to chemical exposures varies greatly among individual organisms and species. Studies in toxicology, which are typically conducted under controlled laboratory conditions, often compare the susceptibility of different organisms to toxic substances. Acute toxicity is defined as occurring when a short-term exposure to a chemical in a high concentration results in biochemical or anatomical damages or even death (a common acute endpoint). Chronic toxicity involves a longer-term exposure to low to moderate concentrations of a chemical. Over time, chronic exposures may cause biochemical or anatomical damage, or perhaps a lethal condition such as cancer.

Data in Table 15.1 illustrate the sensitivities of a number of species to the extremely toxic chemical, TCDD (2,3,7,8-tetrachlorodibenzo-p-dioxin). TCDD has no industrial or medicinal uses, but it is incidentally synthesized during high-temperature combustions in incinerators, during forest fires, in the chlorine bleach whitening process for wood pulp, and in the manufacturing of certain industrial chemicals, particularly trichlorophenol, which is used to produce the herbicide 2,4,5-T and the antibacterial agent hexachlorophene. These syntheses can result in the emission of TCDD into the environment, where humans and other organisms may be exposed. Because of its toxicological notoriety, TCDD and its chemical relatives are relatively well-studied substances.

The data in Table 15.1 suggest that species differ greatly in their sensitivity to TCDD. Among the species for which data are available, the guinea pig is especially vulnerable to TCDD, whereas hamsters and frogs are less so. Sensitivity to chemicals also varies with the route of exposure and with the sex and age of animals.

Table 15.1. Acute Toxicity of TCDD to Various Animals. The animals were exposed to TCDD under laboratory conditions. Oral exposure involves ingestion into the stomach; dermal exposure consist of absorption through the skin; intraperitoneal exposure involves injection into the abdominal cavity. LD50 (lethal dose for 50% mortality) is the dose that kills half of a population of experimental animals. LD50 is measured in units of amount of chemical per unit of body weight (e.g., µg/kg). Source: Data from Tschirley (1986).

Illustrations of data showing acute and chronic toxicities are presented in Table 15.2. The chemical illustrated here is glyphosate, a herbicide that is widely used in agriculture, forestry, and horticulture (see Chapter 22). The data suggest that, if the concentration of glyphosate is large enough, it will cause acute toxicity. However, long-term tests of chronic toxicity did not demonstrate observable effects at the examined levels of exposure. Note also, that the experimental doses needed to cause acute toxicity, and those tested for chronic toxicity, are much higher than exposures that would be encountered during the routine use of glyphosate as a herbicide.

Table 15.2. Acute and Chronic Toxicity of Glyphosate. The toxicity data are from controlled exposures under laboratory conditions. Acute toxicity is measured by the oral LD50, while chronic exposures are from long-term feeding experiments. The data for chronic exposure are no-effect levels, which are doses at or below which there is no observable effect. Source: Modified from Freedman (1991).

2. Inherent Toxicity

Chemicals vary enormously in their intrinsic, or relative, toxicity. Some chemicals are extremely toxic in minute doses, while others will only cause poisoning at a much higher intensity of exposure. This is illustrated by data in Table 15.3, which compares the acute toxicity of a wide range of chemicals. There are two central messages:

• chemicals vary enormously in relative toxicity
• at a large enough dose, any chemical may be toxic

Table 15.3. Acute Toxicity of Various Chemicals. Toxicity is indicated by oral LD50 data from controlled laboratory tests. The LD50 data are in units of mg of chemical per kg of body weight, and the test species was the rat. Source: Data from Freedman (1995).

3. Exposure

Exposure has a fundamental influence on toxicity. It may be defined as the dose of chemical that any individual or group of organisms receives per unit of time. Exposure to any potentially toxic chemical is affected by many factors, including environmental influences. For example, the exposure of a mouse in an agricultural field sprayed with an insecticide could be affected by such factors as the spray rate, kind of equipment being used, weather, persistence of the chemical (how long it remains active), and the behaviour and choices of food and habitat of the mouse. If a toxicologist is evaluating the exposure of people to potentially toxic substances, there would be a consideration of the amount ingested with solid and liquid food, the intake while breathing, and the amounts present in both working and ambient (or non-occupational) environments.

4. Indirect Effects

Also important in ecotoxicology are the indirect effects of toxic chemicals, or effects other than the direct poisoning of organisms. Indirect effects are most commonly associated with changes in habitat or in the condition of the immune system of an organism. In some cases, indirect damage is worse than the direct toxic effects of chemicals. For instance, the use of a herbicide in forestry causes changes in vegetation, which affects animals that live in the habitat, even if the herbicide itself is not directly toxic to them.

All Chemicals Are Toxic

The above discussion suggests that if an exposure is intense enough, even routinely encountered chemicals may be poisonous. In fact, even water can be toxic if a person drinks enough in a short period of time. This happens because the physiological capacity to regulate salts in the blood plasma can be overwhelmed by drinking too much water too quickly, causing a toxic syndrome called hyponatremia. Depending on body weight, the lethal dose for an adult is 5-10 L, ingested over an hour or less. Similarly, if the dose is large enough, carbon dioxide, table sugar (sucrose), table salt (sodium chloride), Aspirin (acetylsalicylic acid), drinking alcohol (ethanol), and other routinely ingested chemicals can cause poisoning (Table 15.3).

This fundamental rule of biology was first emphasized by Philip von Paracelsus (1493-1541), a Swiss physician and alchemist who is considered to be the father of “modern” toxicology. One of his most famous conclusions can be paraphrased as “Dosage determines poisoning.”

In perhaps all cases, there are thresholds of tolerance to potentially toxic chemicals. The tolerance occurs because organisms have physiological mechanisms to excrete toxins from the body, to metabolize them into less-toxic substances, or to sequester (store) them in certain body tissues where they will not cause damage. Organisms also have mechanisms to repair damage caused to tissues or biochemical systems, providing that the chemical exposures are not too high and excessively damaging. For a chemical to cause toxicity, the capacities of these physiological systems must be overwhelmed.

Interpretation of Damage

The notion of physiological thresholds of tolerance helps to define the difference between contamination and pollution, which we examined previously. The idea of thresholds also indicates why it is best to frame the discussion in terms of “potentially” toxic exposures to chemicals. This is especially the case when the actual environmental concentrations are not known, and when the biological risks of extremely small doses are not sufficiently understood. However, the notion of biological thresholds of tolerance is somewhat controversial, and not all toxicologists would agree with the explanation just given. Those scientists believe that exposure to even one or a few molecules of some kinds of chemicals may be of toxicological importance. This is particularly true of chemicals that are thought to be carcinogenic at extremely small exposures, and also of radionuclides and highly energetic forms of ionizing energy, such as X-rays and gamma radiation.

Often, the risks to humans exposed to chemicals are interpreted differently from those of other species, particularly wild animals and plants. This is because the prevailing cultural attitudes place much greater value on the life and health of individual people than on those of other species. As such, there is a special reluctance, both social and regulatory, to permit human exposures to many kinds of potentially toxic chemicals.

However, regulations and guidelines tend to be considerably less strict for human exposures that occur in a workplace, as compared with non-occupational exposures. This recognizes the fact that considerable risks are inherent in the activities and environmental conditions of many occupations. Particularly significant hazards confront firefighters, police officers, members of the armed forces, operators of heavy machinery, and workers in chemical industries. Within limits, chemical exposures associated with earning a living are generally interpreted as a “cost of doing business”, and may therefore be judged to be acceptable.

Such attitudes can, however, change markedly over time. Certain occupational hazards that were once considered routine and tolerable are now viewed as unacceptable. For instance, when synthetic organic insecticides, such as DDT, were first introduced in the mid-1940s and 1950s, people were remarkably casual about using them. Workers often applied these insecticides with only minimal attention to avoiding exposure to themselves and others. Such poorly controlled usages would be unthinkable today, especially in relatively well-regulated countries such as Canada.

In addition, many people willingly choose to expose themselves to toxicologically significant doses of certain chemicals. These choices include taking up hazardous occupations, smoking cigarettes, and ingesting medicines and recreational drugs. The consequences of these sorts of “voluntary” exposures are interpreted using criteria that are different from those applied to “involuntary” ones.

If chemicals cause toxicity to species other than humans, the importance of that effect is interpreted on the basis of the following considerations:

• Are measurable changes seen in the populations of affected species? From an ecological perspective, population-level damage is the most important consideration, even while it is acknowledged that the death of an individual organism is regrettable. Populations of all species have a certain degree of resilience and can tolerate some mortality caused by toxic chemicals without suffering an overall decline.
• Are affected species important in maintaining the integrity of their community? Ecological philosophies suggest that all species have intrinsic value. Nevertheless, species do vary greatly in their contribution to the functioning and structure of their community. So-called keystone species have a dominant influence (Chapter 9). Substantial changes in their abundance should be judged as relatively important compared with damage inflicted on more minor species.
• Is the damage of economic importance? This consideration involves damage to resources that are needed by humans and therefore have economic value. In this sense, damage is judged to be relatively important if it is caused to hunted animals such as deer or trout, to trees that can be harvested to manufacture pulp or lumber, or to vital ecological services such as the provision of clean water and air. From a purely utilitarian perspective, damage caused to non-economic values, both species and services, may be viewed as being less important.
• Other considerations, less tangible than those just mentioned, involve appraising damage in aesthetic or ethical terms. These considerations are also important, but they are difficult to interpret in terms of risks or benefits to human welfare. As a result, aesthetic or ethical considerations are rarely reflected in regulatory criteria or in the management of potentially toxic chemicals in the environment.

Environmental Risks

Broadly interpreted, environmental risks are hazards – a likelihood of suffering damage or misfortune as a result of exposure to a biological or environmental circumstance. Risks are associated with driving an automobile, flying in an airplane, participating in sports, hiking in the wilderness, being exposed to toxic chemicals, and getting out of bed in the morning. Environmental risks interact with biological factors to determine the likelihood of experiencing damage of some kind, such as developing a cancer or suffering an injury.

Statisticians assign probability values to many kinds of risks using data based on previous experience, such as the frequency of automobile accidents or cases of poisoning with a chemical such as a particular medicine. This approach is illustrated in Table 15.4, which summarizes recent causes of mortality in Canada. These data suggest that the average Canadian has an annual risk of dying of about 0.7% (calculated as the total annual mortality divided by the national population).

Table 15.4. Causes of Mortality in Canada. These data summarize the most important causes of deaths among Canadians (in 2011). Source: Data from Statistics Canada (2014).

Data concerning less-common environmental risks are more difficult to acquire. Usually they must be developed from predictive models based on knowledge of medical science and likely exposures to environmental influences. However, both of these kinds of information are imperfect because they are based on an incomplete understanding of interactions between environmental influences and biological responses. Consequentlythe calculated risk factors are inaccurate and sometimes controversial. These issues are particularly important for diseases, such as cancers, that have an extended latency period (often several decades) between exposure and development.

Cancers are a leading cause of mortality in Canada and in other relatively wealthy countries. Remarkably little is known, however, about the specific environmental and biological factors that predispose organisms to developing various types of cancer. Table 15.5 summarizes data from a study that estimated the risks of dying from cancer that are associated with several potentially contributing factors. Of the approximately 0.5 million cancer deaths that occur each year in the United States, dietary factors are believed to be the most important predisposing factor, accounting for about 35% of the mortality, followed by tobacco smoking (30%), infections (10%), and reproductive and sexual behaviour (7%). Of the various risks, smoking is most easily preventable: this voluntary exposure is responsible for about 86% of lung cancers, as well as other diseases (Canadian Cancer Society, 2005). About half of Canadian smokers will die from a smoking-related ailment, most before the age of 70.

The population of Canada is 10.8% that of the United States, while the number of cancer-related mortalities is 11.3% that of the United States. These similar proportions, along with the comparable lifestyles of Canadians and Americans, suggest that the estimated risks in Table 15.5 are also relevant to Canadians.

Table 15.5. Estimated Risks of Cancer Mortality. Cancers are grouped by their possible causes, in terms of environmental exposures. The data are the best estimates for the U.S. population, with the range of estimates in brackets. Sources: Modified from Gough (1989) and Canadian Cancer Society (2008).

Image 15.6. Smoking entails a voluntary exposure to a wide range of chemicals that are known to be toxic. In addition, non-smokers are involuntarily exposed to sidestream smoke by sharing space with smokers in public spaces or their home. Source: B. Freedman.

In spite of excellent data (and common sense) about the known risks of many activities, people often choose to expose themselves to obvious risks of injury or disease. Examples of risky activities include skiing down a steep slope, bungee jumping, smoking cigarettes, and drinking alcohol. Moreover, people are also exposed to hazards over which they have little control – that is, to involuntary risks, such as crime, polluted outdoor air, and pesticides in food. Perceptions of risk are an important consideration. One survey of Canadians indicated that people are aware of and concerned about a wide range of risks to their health and well-being (Table 15.6). People are especially concerned about health-related risks associated with lifestyle choices, such as smoking cigarettes, using recreational drugs or alcohol, and behaviour involving exposure to AIDS (HIV virus). People are also concerned about exposures to potentially toxic levels of chemicals in the atmosphere, drinking water, and foods.

Table 15.6. Public Perception of Risks of Various Environmental and Medical Hazards. The data, based on a national survey of 1503 Canadians, indicate the percentage of the survey group that chose the designated category. The totals do not add to 100% because some respondents said they “didn’t know.” Source: Data from Krewski et al. (2006)

Clearly, people understand that environmental factors pose risks to human health. Often, however, they have little understanding of the actual risks, as opposed to the perceived risks. Sometimes, people view certain high risks to be inconsequential while considering much smaller risks as being unduly important. Nevertheless, public perceptions of risks have an extremely important influence on politicians, policy makers, and bureaucrats in government and industry, and on their decisions concerning the management and regulation of environmental and health hazards.

Environmental Risk Assessment

An environmental risk assessment is an evaluation of the risks associated with a hazard in the environment. A risk assessment may quantify the threats to people, as well as to other species and to broader ecological values. A risk assessment requires knowledge of three factors:

1. the likelihood of encountering the hazard
2. the likely intensity of the hazard
3. the biological damage that is likely to result from the predicted exposure

A meteorologist, for example, may predict the probability that a particular place will be struck by lightning under various weather conditions. The likelihood is much greater during a thunderstorm than during sunny conditions, and is greater beneath a large tree in an open field than beside a shrub in a ditch. The energy content of a typical lightning strike is also known, as is the biological damage to a person who might be struck. With this information, it is relatively straightforward to model the risks of a lightning-caused injury associated with standing in the middle of an open field, or under a tree in that same field, on a sunny day or during a thunderstorm. This is a simple example of an environmental risk assessment. A risk assessment for potentially toxic exposures to chemicals can be conducted for individual organisms, for populations, or for ecological functions such as productivity, decomposition, and nutrient cycling. To assess the risks associated with exposure to chemicals, one requires knowledge of two factors: the intensity of exposure (the anticipated dose) and the biological damage that is likely to be caused by the predicted exposure. The integration of these two types of information is known as a dose-response relationship (Figure 15.1).

Figure 15.1. Conceptual Models of Dose-Response Relationships. Model (a) suggests that the larger the dose encountered, the greater the proportion of the population that is affected. ED50 represents the dose that affects 50% of the test population (effective dose). If the biological response being measured is death, the term LD50 is used, or te dose killing 50% of the population (lethal dose). Model (b) suggests that larger doses have a more pronounced effect on physiology (or on an ecological function). In this case, the rate of a biological function is plotted versus the chemical exposure, and the data are expressed as a percentage of the control rate (in the absence of the chemical). In this curve, ED50 represents the dose needed to decrease the rate of the function by 50%.

A dose-response relationship can be determined by conducting experiments in which, for example, populations of organisms are exposed to various amounts of a chemical. Results of simple dose-response experiments involving several herbicides are shown in Figure 15.2.

Figure 15.2. Examples of Dose-Response Curves. Note the extremely wide ranges of doses that were examined in these experiments. Each experiment includes a control treatment involving a zero dose of the chemical. Graph (a) describes effects of the herbicide 2,4-D on growth rate of a mycorrhizal fungus, Hebeloma longicaudum. Graph (b) illustrates effects of the herbicide 2,4,5-T on the germination of seeds from the surface organic mat of a clear-cut. Graph (c) shows effects of 2,4,5-T on the decomposition of leaf litter. Sources: Data from Estok et al. (1989), Fletcher and Freedman (1989), and Morash and Freedman (1989).

It is sometimes possible to infer dose-response relationships by studying patterns of damage in the real world. For instance, the intensity of pollution can be determined at various distances from a large point source of emissions, such as a power plant or smelter. The exposure to pollution can then be related to the pattern of ecological damage that may be observed along the gradient of toxic stress. Patterns of pollution and ecological damage around a large smelter near Sudbury are one example of such a relationship (see Chapters 16 and 18).

An exposure assessment investigates all of the ways by which organisms may encounter a potentially toxic level of a chemical. For example, humans may be exposed to mercury through various pathways, each of which can be quantified (either measured or calculated using a predictive model). The principal avenues of exposure include: inhaling mercury vapour present in the atmosphere, ingesting mercury dissolved in drinking water, and consuming the metal in foodstuffs, especially in certain kinds of fish and animal organs. Also included among the principal avenues of exposure are miscellaneous sources such as certain pigments used in ceramics and paints, and mercury-amalgam dental fillings.

The assimilation rate of a chemical into the bloodstream and organs varies greatly among the exposure pathways. Assimilation depends on several factors, including the metabolic characteristics of the organ into which the chemical is being absorbed, such as the lungs, the gastrointestinal tract, or the skin. The physical-chemical form of the substance also affects its uptake dynamics. For instance, mercury can occur as an elemental vapour or liquid, as inorganic compounds such as mercuric chloride, and as organomercurial complexes such as methylmercury (an especially bioavailable and poisonous compound). The total exposure for a person is the sum of the chemicals assimilated through all pathways, which typically vary greatly in their effect.

The relative importance of various sources of a chemical depends to some extent on a person’s lifestyle and occupation. These influence how often and to what degree the various sources are encountered. Dental workers, for example, may come into contact with mercury vapours because this metal is sometimes used to make fillings. In addition, a diet rich in certain species of large oceanic fish, such as halibut, shark, swordfish, and tuna, is relatively rich in mercury. Therefore, both dental workers and big-fish consumers may have a higher risk of mercury exposure.

Once an exposure assessment has been undertaken, the biological hazards can be predicted on the basis of known dose-response relationships. Unfortunately, dose-response information is often incomplete, or even lacking. For instance, most hypotheses about potential dose-response relationships in humans are actually inferred from research that has been conducted in laboratories using other mammals, such as dogs, mice, monkeys, pigs, and rats. These species have physiological, anatomical, and behavioural characteristics that are broadly similar to those of humans, but they also differ in important respects. Consequently, most assessments of human exposure to trace levels of environmental chemicals are inaccurate.

In addition, the information about dose-response relationships is almost non-existent for wild species and for ecological functions such as productivity and nutrient cycling. As with human-focused assessments, it is common to use data for surrogate (or proxy) species, which are believed to be typical in their dose responses.

For example, a study may be undertaken to predict the potential effects of inputs of particular chemicals to a certain lake. It is highly unlikely that relevant dose-response data will be available for the species of fish in the ecosystem. Consequently, predictions will typically be made using information for proxy species, such as rainbow trout (Salvelinus gairdneri) or fathead minnow (Pimephales promelas). These fishes have been well studied in toxicological laboratories and are widely used as indicators. Similarly, the potential effects on the zooplankton community might be predicted using information available for well-studied species, such as the water fleas Daphnia magna and Ceriodaphnia dubia, while the risk assessment for phytoplankton might use data for the unicellular algae Selenastrum capricornutum and Chlorella vulgaris.

The results of a risk assessment for an ecosystem or a part of it (such as a community), if based on laboratory studies of surrogate species, are always uncertain. This is especially true if the potential effects are being predicted of chemical exposures in a natural environmental context. Such risk assessments are, however, the best that can be done under most circumstances because there is rarely enough funding or time to do more comprehensive studies. Nevertheless, because these methods deliberately overestimate the potential risks, they provide conservative guidance for management purposes.

In Detail 15.2. Mutagens, Teratogens, and Hormone Mimics Mutagens, teratogens, and hormonally active substances are trace chemicals and other agents that are present in the environment and have the potential to affect the genetics or metabolism of animals when present in minute concentrations. They may be naturally present or associated with anthropogenic emissions. Relatively intense exposures of wild animals to these agents may occur in aquatic habitats that are affected by effluent from factories, sewage, or pesticide-treated fields. Human exposures are associated with smoking (including involuntary exposures), eating fatty meats (especially if barbequed) and some other foods, and living in an urban environment that is generally polluted with a range of substances.

A mutagen is a substance or agent that induces a genetic mutation, meaning a change in the coding sequence of nucleic acids in DNA or RNA. Exposure to mutagens may result in mutations that are “harmless,” meaning the genetic change is not known to result in a serious biochemical consequence. In other cases, however, a mutation may result in a deformity or disease, such as many kinds of cancer. A cancer may be an endpoint of mutations occurring in body (somatic) cells, while mutations of sperm and egg cells may result in heritable changes that can be passed to offspring. An environmental mutagen is one that is encountered in the environment. Incidents of genotoxicity have been observed in wild animals, such as occurrences of fish tumours and frogs born with excess limbs. In humans, genotoxicity may be associated with some kinds of cancer and with congenital birth defects, which normally occur in about 3% of births. Genotoxocity may be caused by exposure to various chemicals and other agents. Potent mutagens that are used in biomedical research include ethylmethanesulfonate and nitrosoguanidine. Other sources of laboratory and environmental genotoxicity include the following:

• highly energetic (ionizing) radiation associated with ultraviolet-B, X-rays, and gamma radiation
• polycyclic aromatic hydrocarbons (PAHs), such as benzo(a)pyrene
• polychlorinated biphenyls (PCBs) and certain pesticides
• methyl mercury and some other metals
• aflatoxin present in mouldy nuts and grains
• dimethyl nitrosamine present in nitrite-treated foods
• diesel exhaust
• effluent from pulp mills
• tobacco and barbecue smoke

A teratogen is an agent that induces abnormal development of an embryo or fetus. It may act through mutagenicity or by some other means, such as physical irritation of cells or tissues. A famous example of teratogenic damage was caused by thalidomide, a medication that was prescribed as a sedative to pregnant women from 1950-1961. Thalidomide proved to be capable of crossing the placenta and caused devastating limb abnormalities (extreme shortening or absence of limbs) in the fetus, and its medical use resulted in an epidemic of seriously deformed children. Another well-known teratogen is ethyl alcohol (alcohol in drinks), which if taken in excess during pregnancy can cause fetal alcohol syndrome. Exposure to rubella virus during pregnancy can also lead to severe deformity of a fetus. An environmental teratogen is encountered in the environment, and this exposure may have increased the incidence of deformities of wild animals, including mollusks, fish, and amphibians.

A hormonally active substance is a hormone or another chemical that has a similar effect on the regulation of biochemistry. Hormones are chemical messengers that travel through the circulatory system until they reach specific receptor cells in target organs, where they regulate physiology. They are produced in the endocrine system, which consists of various glands, such as the adrenal gland, ovaries, pancreas, pituitary gland, testes, and thyroid gland. Hormones help to regulate growth, development, metabolism, deposition of fat, maintenance of the electrolyte balance in fluids, sexuality, and behavioural responses to external stimuli (such as excitement and fright). Examples of hormones include the following:

• adrenaline (epinephrine) and noradrenaline (norepinephrine), which are adrenal hormones that stimulate the body to react to a stressful condition by increasing the blood pressure, blood sugar, and heart rate (this is sometimes known as a “flight or fight” response)
• estrogen, a female sex hormone produced by the ovaries, and androgens, male hormones produced by the testes
• insulin, formed by the pancreas to regulate the use and storage of carbohydrates (including blood sugar)
• thyroid hormone, which influences the growth and metabolism of virtually all body cells

Because hormones are necessary for healthy physiology, development, and behaviour, any serious disruption of their activity can have severe consequences for organisms. Some chemicals present in the environment, including natural ones and others that are anthropogenic, can cause such interference and are known as hormone mimics. For example, certain plants contain so-called phytoestrogens that can affect the hormone physiology of animals feeding upon them. Examples of plants with relatively high levels of phytoestrogens include soybean (Glycine max), red clover (Trifolium pratense), flax (Linum vulgare), and black cohosh (Cimicifuga racemosa). Some women use herbal preparations of these plants to relieve symptoms of menopause. Other natural phytoestrogens have been used in birth-control pills to control human fertility.

Many other substances present in the environment are also hormonally active, including a wide array of chemicals released by human activities. Even at extremely small exposures, they may mimic or block the action of certain hormones, resulting in a physiological change. This may have detrimental effects on wild and domestic animals and also on people. The following anthropogenic chemicals are thought to be hormonally active through environmental exposures:

• organochlorines, including dioxins (such as TCDD), polychlorinated biphenyls (PCBs), and the insecticides DDT, dieldrin, and lindane
• other kinds of pesticides, including atrazine, permethrin, and trifluralin
• tributyltin, which is used as a marine antifoulant
• alkylphenols used as surfactants, such as nonylphenol
• certain placticizers, such as dibutyl phthalate and butylbenzyl phthalate
• natural hormones and synthetic steroids from contraceptives that are released to the environment in sewage or occur as residues in food, including estradiol, estrone, and testosterone
• phytoestrogens in pulp-mill effluents, including coumestans, isoflavones, and lignans

The biological effects of environmental mutagens, teratogens, and hormonally active substances are not yet well understood. Although the presence of many of these agents in the environment has been widely noted, scientists do not yet know the level of contamination at which an unacceptable amount of biological damage may result. This has resulted in controversy about the potential effects of these bioactive chemicals on wild animals and humans: some people recommend a highly precautionary approach, while others believe that more evidence of consequential damage is needed before stringent control practices are implemented. Although there are observations of some local populations of wild animals suffering significant damage, there is not yet convincing evidence of effects on people from environmental exposures to these agents. Of course, any significant level of genetic or developmental damage to humans would be deemed to be unacceptable.

References: Phillips and Venitt (1995), Machachlan and Guillet (2002), Servos et al. (2008)

Mercury in Aquatic Environments

Even in remote oceanic habitats, mercury often accumulates in high concentrations (as methylmercury, CH₃Hg) in fish, birds, and sea mammals. In marine waters off eastern and western Canada, large fish may have mercury concentrations in their flesh that exceed the limit considered acceptable for human consumption (more than 0.5 ppm mercury on a fresh-weight basis; Figure 18.1). Analysis of old specimens of fish and seabirds in museums has revealed levels of mercury contamination similar to those in modern samples, which suggests that the phenomenon may be natural. The contamination of marine animals represents a substantial biomagnification from ambient seawater, which has a trace concentration of mercury of less than 0.1 ppb.

Figure 18.2. Mercury Contamination of Fish Captured Offshore of North America. The data show the average mercury concentration in the muscle of species of marine fishes. The data are in ppm, measured on a fresh-weight basis. Source: Data from Armstrong (1979)

The biomagnification occur because of the progressive accumulation of mercury up the trophic web. Algae initially absorb mercury from the water (as methylmercury), and zooplankton accumulate even larger residues as they graze on the algae. Zooplankton-eating fish accumulate still larger quantities, but the largest residues occur in long-lived top predators, such as big fish and marine mammals (see In Detail 18.1).

Within any particular species of fish, larger (and older) individuals generally have higher mercury concentrations than smaller (and younger) ones. A study of swordfish caught off eastern Canada found that animals heavier than 45 kg had an average mercury concentration of 1.1 ppm, while those weighing 23-45 kg had 0.86 ppm, and those smaller than 23 kg had 0.55 ppm (Armstrong, 1979). It appears that mercury residues become more intense as the animals age and grow larger.

High concentrations of mercury also occur in fish-eating marine mammals and birds, which are top predators in their ecosystem. Studies of adult harp seals (Phoca groenlandica) in eastern Canada found an average mercury concentration of 0.34 ppm in muscle and 5.1 ppm in the liver (Armstrong, 1979). High mercury residues also occur in North Atlantic seabirds, with an average of 7 ppm found in feathers of northern skua (Catharacta skua), 5 ppm in puffin (Fratercula arctica), and 1-2 ppm in fulmar (Fulmarus glacialis), kittiwake (Rissa tridactyla), razorbill (Alca torda), and common murre (Uria aalge) (Thompson et al., 1991).

Mercury contamination of fish has also been observed in many remote lakes. For example, about three-quarters of 1,700 lakes monitored in Ontario have fish with mercury exceeding 0.5 ppm fresh weight in their flesh. In a remote lake in northern Manitoba, the average mercury concentration in muscle of 53 northern pike (Esox lucius) was 2 ppm fresh weight and one animal had 5 ppm (McKay, 1985). In general, freshwater fish that are top predators have the highest residues of mercury, and larger or older individuals are the most contaminated.

Federal, provincial, and territorial governments in Canada issue advisories about eating fish taken from particular lakes and rivers where mercury residues are known to be a problem; the advisories may also have information about other contaminants, such as PCBs and dioxins. In Ontario, for example, more than 2,200 waterbodies are monitored for this purpose (MOEE, 2014). The advisories tell people how many fish of particular species and sizes they can eat. The general threshold is 0.61 ppm, but it is as low as 0.26 ppm for pregnant women and children, and no fish with more than 1.84 ppm should be consumed. About one-third of the advisories given for sportfish taken from Ontario lakes result in some level of consumption restriction. In Sweden, about half of the lakes have some fish with mercury exceeding the health advisory limit (0.5 ppm), and hundreds of lakes have been blacklisted because their fish are considered unfit for human consumption.

The causes of mercury contamination of lakes are not known for certain. It seems likely that the phenomenon may be natural in regions that are remote from sources of emission. However, anthropogenic mercury is contributing to the problem closer to large emissions sources, such as coal-fired generating stations, municipal incinerators, and smelters. For example, Harp Lake in Ontario is located relatively close to municipal and industrial sources of emissions. Studies found that atmospheric deposition accounted for 57% of the mercury input to that lake, suggesting a significant anthropogenic influence (Mierle, 1990).

The above discussion of mercury in lakes refers to the many situations in which there are no direct anthropogenic inputs of the metal. However, there are well known cases of pollution caused directly by industrial releases. For example, discharges from chlor-alkali and acetaldehyde factories and some older pulp mills have caused local mercury pollution, resulting in high residues of methylmercury in fish and other animals. The case of Minamata Bay, Japan, involved an acetaldehyde plant (Global Focus 18.1). A less severe case in Canada, which affected parts of the English and Wabigoon Rivers in northwestern Ontario, involved a pulp mill.

Significant bioaccumulation of mercury also occurs when hydroelectric reservoirs are developed (see Chapter 20). Flooding leaches naturally occurring soil mercury into the reservoir, where bacteria in oxygen-poor sediment transform it into methylmercury that is biomagnified by fish. This process occurs more rapidly in acidic lakes because that condition favours the production of methylmercury in the sediment, compared with less available dimethylmercury in non-acidic waterbodies.

Although there is some controversy about the relative importance of natural and anthropogenic sources of mercury to remote lakes, it is reassuring to know that the overall emissions have been greatly reduced in recent decades (Figure 18.3). This occurred because of improved emissions controls at industrial facilities, including the closing of several metal smelters and coal-fired power plants.

Figure 18.3. Mercury Emissions in Canada. Source: Data from Environment Canada (2015).

Global Focus 18.1. Mercury in Minamata Bay
Minamata is a city in Japan where industrial emissions from a factory caused a famous example of toxic pollution, beginning in the 1950s. The factory produced acetaldehyde, which is used to make plastics. The industrial process used inorganic mercury as a catalyst, and between 1932 and 1968, about 25 tonnes of the metal was dumped into Minamata Bay with wastewater discharges. Bacteria in anaerobic sediment transformed the mercury into methylmercury, which became biomagnified in fish to resides as high as 20 ppm. The fish were eaten by predatory birds, causing toxicity and reproductive failure. Fish and shellfish were also harvested and eaten by people living around the bay, which has a long-standing, traditional fishing economy. This caused an episode of toxicity that became known as “Minamata Disease.”

It took several years for the complex of symptoms caused by methylmercury poisoning to be recognized as being ultimately due to emissions from the acetaldehyde factory. Initially, in the mid-1950s, doctors noticed that people were displaying a novel and strange neurological syndrome, characterized by progressive degeneration of the nervous system. Symptoms intensified from numbness in the limb extremities, to slurred speech, loss of peripheral vision, convulsions, unconsciousness, and ultimately the death of many victims. There was also a congenital syndrome caused by toxicity to fetuses by methylmercury passed across the placental barrier. Afflicted children suffered from deformity, mental retardation, and impaired motor control. At the same time, fish-fed cats were killed by a neurological disease, as were fish-eating birds.

It soon became apparent that the disease was being caused by eating fish harvested from Minamata Bay. Although industrial waste being dumped into the bay was an early suspect, not much was initially done to either reduce the discharges or to prevent people from eating seafood caught in the polluted area. Then, in 1959, scientists from Kumamoto University concluded that an organo-mercurial compound was the cause of the toxic syndrome. Soon after, it was realized that its origin was inorganic mercury of industrial origin that was being naturally methylated in the bay. The company that caused the pollution challenged these conclusions, although it began to pay compensation to some of the most severely afflicted people (but only if a release was signed that absolved the company of responsibility and eliminated the possibility of future lawsuits; moreover, many affected people were denied compensation). Despite intense controversy, the company continued to release mercury to the aquatic environment until 1968, when a change in technology eliminated it from the manufacturing process.

Ultimately, about 2,200 people were officially diagnosed as having Minamata Disease as a result of exposure to methylmercury in seafood harvested from the bay. Of these, about 100 died of their poisoning. In addition, at least 12-thousand people may have suffered milder forms of the disease but were not officially diagnosed. In 1973, a court found the chemical company to have behaved in a negligent manner and to be liable for the damages. Many people suffering from mercury-caused disease were awarded compensation, although the amounts paid were disputed as being insufficient and many people received nothing. The bottom line, however, is that people died of avoidable methylmercury poisoning, and many survivors experienced terrible physical and mental disabilities.

Important lessons can be learned from this environmental catastrophe. One is that unanticipated consequences may result from human activities that are thought to be environmentally safe. In the Minamata case, it was believed that the dumping of wastewater containing inorganic mercury would not cause serious damage to the marine environment. At the time, it was not known that bacteria in sediment are capable of transforming mercury into bio-magnifying and toxic methylmercury. Moreover, even when it was recognized that this was happening, and that people and wildlife were being poisoned, business interests and regulatory and political authorities did not act decisively to ensure that people were no longer exposed to the toxic threat. This negligence greatly compounded the problem.

In any event, the tragic case of Minamata Bay has improved our understanding of the consequences of discharging mercury into an aquatic environment. However, the broader lesson about unintended consequences of poorly considered economic activities is not yet firmly enshrined in our planning and regulatory systems.

Examples of Pollution Sources

Industrial processes used to mine, process, and use metals can result in the pollution of air, water, and land (refer to Figure 13.1).

Mining Residues

Areas near mine sites may be badly damaged by the dumping of metal-rich excavation waste (rocks whose metal concentration is not high enough to be considered commercial ore). Because these materials may be toxic, vegetation development can be restricted to early successional communities, such as sparse grassland. In some cases, soil toxicity is severe enough that few plants manage to establish even after hundreds of years. This can be seen on mine wastes from 2000-year-old Roman lead workings in England and Wales.

Ecologists studying British sites polluted by mine wastes have found that these habitats often support plant ecotypes that are genetically tolerant of the metals that are present. The locally adapted ecotypes can grow in metal-polluted soils, where non-tolerant plants are eliminated by the toxic stress. Conversely, the tolerant ecotypes are poor competitors in non-polluted environments, and so are rare in habitats unaffected by metal toxicity.

Research into metal-tolerant ecotypes has provided insights into the process of evolution. Metal-tolerant individuals do occur in populations growing on non-polluted sites, but they are rare. However, the frequency of tolerant genotypes increases quickly after metal pollution occurs. In places with sharp boundaries between polluted and non-polluted soils, a tolerant population can maintain itself over a distance of only a few metres. This is possible because the intense toxicity of polluted soil strongly favours the survival and reproduction of tolerant individuals. Such a population-level change in genetically based characters, occurring in response to an agent of natural selection (in this case, metal pollution), is a demonstration of evolution (more specifically, microevolution).

Metal-tolerant ecotypes have been studied near Sudbury, where pollution by nickel and copper has been caused by emissions from smelters and roast beds. Plant communities of polluted sites are dominated by metal-tolerant ecotypes of several grasses, particularly Agrostis gigantea and Deschampsia caespitosa. Meadows of these grasses developed soon after the extremely tall “superstack” was commissioned in 1972. Because it dispersed emissions widely, the superstack greatly reduced ground-level SO₂ pollution. However, soil in the area remained acidic and polluted with metals. The local ecotypes of these grasses can tolerate toxic stress from acidity and metals, but are intolerant of SO₂, which is why the grasslands did not develop until after the superstack began to operate.

The metal tolerance of the grass Deschampsia caespitosa has been studied. Plants were grown in solutions containing the metals of interest, and were compared with controls (Figure 18.3). The data show that the Sudbury population is tolerant of nickel and copper, which occur in their native soil at concentrations of about 400 ppm, compared with 20 ppm at non-polluted reference sites. The Sudbury population is also more tolerant of aluminum. This is a response to the greater solubility and toxicity of aluminum in acidic soil near the smelters (which had a pH of 3.5-3.9, compared with pH 6.8-7.2 at reference sites).

Figure 18.4. Tolerance of a Grass to Metals. Populations of the hairgrass (Deschampsia caespitose) were collected from metal-polluted places near Sudbury and from reference sites where metals are not a problem. The index of metal tolerance is based on the root growth that occurs when plants are grown in solutions containing metals, compared with a no-metal control. The larger the index number, the greater the tolerance. In all comparisons presented here, the two populations had statistically significant differences in tolerance to the metal tested, with a probability level of <0.001, except for aluminum (p < 0.05; note: a probability value of <0.001 means that there is less than a 0.1% (or 1/1000) likelihood that the difference between the two populations is due to chance alone; p <0.05 means there is less than a 5% chance). Source: Data from Cox and Hutchinson (1979).

Metal-Containing Tailings

Once ore is mined, it is ground to a fine powder in a process called milling. The powder is then separated into a valuable metal-rich fraction, which is roasted and smelted, plus large quantities of waste tailings. In most cases, the tailings are dumped into a low-lying contained area, which when full is covered with vegetation as a stabilization measure. Although the tailings are a waste product, they still contain high concentrations of metals, and that can make it difficult to establish vegetation after a dump is filled. In addition, if sulphide minerals are present, acidity is generated when they become oxidized by bacteria, and that makes the toxicity worse. Chemical analyses of tailings from several Canadian mines are shown in Table 18.2. The tailings contain high concentrations of various metals, depending on the ore being processed. The acidic tailings are especially toxic, because metals are much more soluble and bioavailable under acidic conditions.

Table 18.2. Chemical Analyses of Metal-Contaminated Tailings. Samples were taken from sites in the Yukon and northern Ontario. Metal data are in ppm, sulphur in %. Data modified from Kuja (1980).

Canadian regulators require that tailings-disposal areas be covered with vegetation once they are full of waste or after their associated mine closes. This is done because tailings dumps have poor aesthetics and can be sources of wind-borne dust. These environmental problems can be substantially mitigated if an abandoned tailings dump is covered with a stable cover of vegetation. In addition, if their associated dams and berms are not structurally sound and become breached by high water flows during severely rainy weather, tailings-disposal areas can be a source of massive water pollution.

One such disaster occurred in 2014 in the Cariboo region of central British Columbia, when an accidental breach occurred at the tailings disposal area of a copper- gold mine at Mount Polley. The massive spill involved about 10-million cubic metres of water and 4.5-million cubic metres of slurry (a fluid mixture of tailings particles and water) (Allen and Voiland, 2014). The great scouring flow eroded banks and uprooted trees and much of the volume eventually deposited into nearby Polley Lake, whose surface rose by 1.5 metres. Some of the flow then continued via Hazeltine Creek into the much larger Quesnel Lake, which had been famous as a deep, pristine waterbody. By the end of the day of the breach, the 4-km2 tailings pond was almost empty. In this case, the cause of the breach appears to have been over-filling of an under-engineered tailings disposal area.

Image 18.2. A catastrophic release of tailings occurred at the Mount Polley mine in 2014. The top image shows the tailings-disposal area prior to the breach, with the light-blue colour representing the area where wastes were being dumped. The bottom image shows conditions after the breach, with almost all of the volume of the dump site having escaped to Polley Lake and some also to Quesnel Lake. Source: NASA (2014).

If a filled-up tailings-disposal area is to have a stable cover of vegetation established on top, its contents must be treated to reduce the toxicity. If the tailings are acidic, a liming treatment is needed to raise the pH to a neutral level and so reduce the availability of metals. Fertilizer may also be used to alleviate nutrient deficiency and organic matter added to improve soil structure and water-holding capacity, and then plants are sown. Sometimes, novel techniques are used, such as the use of acid- or metal-tolerant ecotypes in the planting mixture. If the tailings are extremely toxic or acid-generating, they may have to be covered with a locally available overburden, such as glacial till, which is then vegetated. Canadian Focus 18.1 describes the reclamation of tailings-disposal areas in the vicinity of Sudbury.

Image 18.3. Tailings are the fine waste that remains after ore is ground and processed to remove metal-rich minerals. Tailings contain high concentrations of metals and can generate acidity when exposed to the atmosphere. These conditions make it difficult to establish vegetation after disposal sites are filled. This is a view of a reclaimed area of tailings near Sudbury. Most of the vegetation was sown, but native shrubs and trees are also becoming established. Source: B. Freedman.

Canadian Focus 18.1. Tailings Reclamation at Copper Cliff
A large smelter at Copper Cliff, near Sudbury, is serviced by a mill that produces large amounts of tailings (54-thousand tonnes per day at the time the case study of Peters (1984) was written). The tailings are mixed with water and piped as a slurry to be disposed in natural basins whose capacity is increased by the construction of earthen dikes. In 2005, the tailings dumps covered about 3,025 ha, of which 1,425 ha had been stabilized by a cover of perennial vegetation. The vegetation prevents fine dust from blowing into the atmosphere and improves aesthetics and environmental quality. The re-vegetated tailings areas have a central pond, which is surrounded by gradually sloping grassland.

The tailings are a finely ground material, composed mainly of minerals that are not particularly toxic. However, the tailings contain pyrites that oxidize when exposed to atmospheric oxygen, and generate acidity as low as pH 3.7. These extremely acidic conditions result in metals becoming available for plant uptake, which greatly increases the toxicity of the tailings. Plant-available metals were analyzed by extracting tailings with acetic acid, and very high levels of available metals were found, with nickel up to 87 ppm, copper 81 ppm, and iron 440 ppm.

The reclamation procedures result in a stable grassland being established, which is then invaded by native shrubs, trees, and other plants. The methods include the following:

1. application of 900 kg/ha of limestone (CaCO₃), which raises the pH of the tailings to 4.5-5.5 and reduces the availability of metals
2. several applications of fertilizer during the initial stages of grassland establishment, with nitrogen being especially important
3. application of an organic mulch to improve the water-holding and aeration characteristics of the surface tailings
4. sowing with a mixture of long-lived pasture grasses and legumes, as well as annual rye (Secale cereale), which provides a short-lived nurse crop that helps mitigate the stressful microclimate for tender seedlings of the perennial grasses and legumes

As vegetation establishes and develops on the reclaimed tailings-disposal areas, some animals begin to use the habitat. Birds that breed in the grassy habitat and its central pond include mallard and black ducks (Anas platyrhynchos and A. rubripes), American kestrel (Falco sparverius), killdeer (Charadrius vociferus), and savannah sparrow (Passerculus sandwichensis). At least 90 species of birds have been observed to use the reclaimed tailings dump and its pond during migration.

Smelters

A smelter is a large industrial facility where ore is roasted. This is done to oxidize sulphide minerals, a process that results in large amounts of waste SO₂ and metallic particulates. In most cases today, pollution-control technologies are used to recover much of the SO₂ and particulates before the flue-gases are vented to the atmosphere. In the past, however, those wastes were emitted into the environment, causing intense pollution and ecological damage. As recently as several decades ago this was a common practice, and it still is for some older smelters. Newer smelters operate much more cleanly.

A smelter is a point source of toxic stress to surrounding ecosystems. Emissions may result in well-defined spatial gradients of both pollution and its resulting ecological damage, which diminish with increasing distance. Studies of damage near smelters indicate the following generalizations:

• Close to the point source, pollution by atmospheric SO₂ and metals in soil is most severe
• The intensity of pollution decreases rapidly (more or less exponentially) with increasing distance from the smelter.
• Damage to vegetation varies with the intensity of toxic stress and includes decreases in biomass, productivity, and species diversity, with only a few low-growing species occurring in the most polluted habitats
• Ecological processes such as nutrient cycling and decomposition are disrupted by toxic metals, gases, and acidity

The pattern of metal pollution around a point source can be illustrated by the Copper Cliff smelter near Sudbury. Figure 18.4 shows that metal concentrations in the environment decline rapidly with increasing distance from that smelter. These data specifically refer to the forest floor, but similar observations are seen in soil, vegetation, lakewater, and other components of the ecosystem.

Figure 18.5. Metal Pollution near Sudbury. Decades of emissions of metals from the Copper Cliff smelter caused an accumulation of nickel and copper in the environment. The most intense pollution occurs close to the point source. These data are for metals in the forest floor, which is the organic-rich layer that overlies the mineral soil. The forest floor binds metals in organic complexes and accumulates higher residues than the underlying soil. The samples were collected along a transect running south from the smelter. The spatial patterns of copper and nickel are highly correlated, with a coefficient of 0.98. Source: Data from Freedman and Hutchinson (1980).

SO₂ has also been an important pollutant in the Sudbury area. Consequently, it is difficult to determine the specific role of toxic metals in causing ecological damage. One way to investigate the influence of metals is to grow plants in polluted soil in a greenhouse, where SO₂ is not present. These bioassay experiments have demonstrated that soil collected near the smelters is toxic, mainly because of its high concentrations of metals. To a substantial degree, the toxicity persists even after the soil acidity is neutralized by adding lime.

Not all smelters emit both SO₂ and metals. The ecological damage that results from those that emit only metallic particulates has consequently been caused by metal pollution. One well-studied smelter, at Gusum, Sweden, has operated since 1661 (Tyler, 1984). Zinc is an important pollutant there, reaching concentrations as high as 2% (20-thousand ppm) in surface organic matter close to the point source, compared with less than 200 ppm farther than 6 km away. Copper pollution is similar, reaching 1.7% within 0.3 km, compared with 20 ppm beyond 6 km. The zinc and copper pollution has caused local ecological damage. Pine and birch trees have died or declined close to the source, and understorey plants, mosses, lichens, and soil-dwelling invertebrates have been damaged. Rates of decomposition and nutrient cycling are also impaired in the most polluted sites. Some plants, however, are tolerant of the metal pollution at Gusum. They include the grass Deschampsia flexuosa and the moss Pohlia nutans, which do relatively well in sites that are toxic to other plants.

Use of Inorganic Pesticides

Until the 1970s, inorganic chemicals were widely used as pesticides in agriculture (see also Chapter 22). This was especially true in fruit orchards, where pesticides based on lead arsenate, calcium arsenate, copper sulphate, and related compounds were used to control fungal diseases and arthropod pests. These compounds have now been largely displaced by synthetic organic pesticides.

However, until the mid-1970s, annual spray rates of lead in Ontario orchards were as high as 8.7 kg/ha, while arsenic treatments reached 2.7 kg/ha, zinc 7.5 kg/ha, and copper 3.0 kg/ha (Frank et al., 1976). The spray rates depended on the crop being grown, the pest being managed, and the pesticide used, but in some cases all of these toxic elements were applied in the same orchards.

Residues of these chemicals accumulated in the soil of treated orchards. Studies of apple orchards found residues as high as 890 ppm of lead and 126 ppm of arsenic in surface soil, compared with background levels of <25 ppm lead and <10 ppm arsenic (Figure 18.5). The accumulations were caused by up to 70 years of spraying lead arsenate as an insecticide, mostly against the codling moth (Laspeyresia pomonella), a pest that causes “wormy” apples.

Figure 18.6. Accumulation of Arsenic and Lead in Orchards. Lead arsenate was used as an insecticide to combat infestations of apple orchards with codling moth. These data show the progressive accumulation of arsenic and lead in soils of orchards in southern Ontario. The largest residues are in the oldest orchards, which had been sprayed for many years. The background concentration for lead is 20 ppm, and for arsenic it is 10 ppm. Source: Data from Frank et al. (1976).

Agricultural soil can also be contaminated by the use of mercury-containing fungicides, especially those that protect newly germinated seedlings from a fungal infection known as damping-off. This pathogen attacks seedlings at the soil-air interface and causes the weakened plant to fall over and die. Mercury-containing pesticides are also used to control turfgrass diseases on golf-course putting greens. Mercury residues ranging from 24-120 ppm have been measured in the soil of putting greens in Ontario, while up to 9 ppm was found in Nova Scotia. The sowing of seed coated with mercuric fungicide has caused poisoning of wild animals that consumed the planted grain or ate herbivores that did so. Alkyl-mercury compounds such as methylmercury are especially hazardous in this respect because this form is extremely toxic and readily assimilated by animals from their food. Figure 18.6 shows the mercury contamination of seed-eating wildlife in regions of Alberta where treated seed was used, compared with areas where that exposure did not occur. Use of these fungicides was common until the early 1970s.

Figure 18.7. Mercury in Animals Feeding on Treated Seed. Seed-eating rodents and birds were exposed to alkyl-mercury fungicide by feeding on treated seed in agricultural areas in Alberta. Data are also presented for an area where mercury-treated seed was not used (labelled as untreated). The data are average data for liver and are in ppm dry weight. Source: Data from Fimreite et al. (1970).

Beginning in the late 1960s, most developed countries prohibited the use of alkyl-mercury fungicides as seed dressings. This ban resulted from the recognition of ecological problems associated with use of these chemicals, especially the poisoning of wild animals. Sweden, for example, prohibited the use of these pesticides in 1966, while approving the use of alkoxyl-alkyl-mercury compounds, which are much less toxic, as replacements. This action rapidly led to decreased mercury contamination of wildlife, such as predatory birds (Figure 18.7). Canada took similar action, although several years later.

Figure 18.8. Mercury Contamination of Swedish Hawks. (a) Mercury in feathers of goshawks (Accipiter gentilis), during various time periods; (b) Mercury in feathers of marsh harriers (Circus aeruginosus). Note the large increase in contamination caused by the use of alkyl-mercury fungicides and the rapid decrease that followed the banning of these chemicals in 1966. Source: Data from Johnels et al. (1979).

As was noted in the introduction to this chapter, humans have also been poisoned by inadvertently eating mercury-treated seed grain.

Birds and Lead

Millions of birds have suffered lead poisoning in North America each year because they ate spent shotgun pellets. Most of the spent shot was associated with hunting. In Canada, for example, about 2000 tonnes of lead shot were used by hunters each year in the early 1990s. Although more localized, skeet shooting was also a problem because of the large amount of shot deposited, up to tonnes of lead each year.

After being ingested by a seed-eating bird, lead shot may be retained in the gizzard, a muscular forepouch of the stomach. Hard grit is normally retained in the gizzard and used to grind tough-coated seeds, aiding in their digestion. Unfortunately, shotgun pellets are similar in size and weight to the grit that many birds select for this purpose. The shot becomes abraded in the gizzard, and the bits are swallowed and dissolved by acidic stomach fluid. The lead is then absorbed into the bloodstream, allowing it to poison the nervous system of the bird, leading to death.

Waterfowl have been especially widely affected, with 2-3 million individuals, or 2-3% of the North American population, dying each year from lead-shot poisoning in the early 1990s. The retention of just one or two pellets in its gizzard can poison a duck, causing a wasting away of 30-50% of its body weight, neurological toxicity, and ultimately death. Typically, about 10% of the waterfowl surveyed in North America had one or more shotgun pellets in their gizzard. Larger aquatic birds, such as swans, are known to retain lead fishing weights in their gizzard. Lead sinkers or shot were cited as the cause of 20-50% of the mortality of trumpeter swans (Cygnus buccinator) in western North America. Lead sinkers are also known to poison tundra swans (C. columbianus) wintering in the eastern United States, mute swans (C. olor) in Europe, and common loons (Gavia immer) in Canada and the United States. In Canada, about 500 t/y of lead fishing sinkers and jigs were lost in the early 1990s.

A related syndrome, caused by ingesting lead shot and bullets, afflicts birds that scavenge dead carcasses. Although the numbers are not well documented, this poisoning is known to kill vultures, eagles, and other scavenging birds. The critically endangered California condor (Gymnogyps californianus) has been relatively well studied – about 60% of its known deaths in the wild between 1980 and 1986 were caused by toxicity from ingested bullets in carrion. Because of the widespread poisoning of birds by lead shot, regulators have now restricted its use. Lead shot is banned over most of the United States. In Canada, the use of non-toxic shot has been required in all wetland areas since 1997 and in all other hunting areas since 1999. The use of lead shot for hunting is being replaced mostly by steel shot, and to a lesser degree by bismuth shot. The restricted use of lead shot has caused some controversy because many hunters believe that the alternative shot types might cause more crippling deaths. However, field tests have shown this effect to be marginal, as long as the inferior ballistic qualities of the alternatives are compensated for by shooting at closer distances or by using a larger size of shot.

Automobile Emissions of Lead

Lead emitted by automobiles has contributed to a general contamination of urban environments. From 1923, but particularly after 1945, tetraethyl lead was added to gasoline as a so-called “anti-knock” compound. The lead increases mechanical efficiency and gasoline economy, while decreasing engine wear. In 1975, about 95% of the gasoline used in North America was leaded at concentrations as high as 770 ppm. In 1987, only 35% of the gasoline was leaded, and the maximum permitted then was 290 mg/L. The decreased use of lead between 1975 and 1987 was mostly due to the increased use of catalytic converters to reduce emissions of other automobile pollutants, especially carbon monoxide and hydrocarbons. Automobiles equipped with a catalytic converter can only use unleaded gasoline, because the catalysts, usually platinum, are rendered inactive by lead. The increasing use of unleaded fuels resulted in a 93% decrease in lead particulates in the air of Canadian cities between 1977 and 1989.

After 1990, the use of leaded gasoline was banned in Canada and the United States (the only exceptions were low-lead fuels [up to 30 ppm] for use in some farm vehicles, marine engines, and large trucks). Consequently, emissions of lead from automobiles in Canada decreased from about 9,500 t in 1978 to less than 100 t/y since 1995. However, many other countries, particularly in the less-developed world, continue to allow the use of leaded fuels.

Almost all of the lead in gasoline is emitted as particulates through the vehicle tailpipe. The larger particulates settle out close to the roadway. This results in the buildup of a well-defined gradient of lead pollution, the intensity of which is related to traffic volume. This pattern of roadside pollution is illustrated in Figure 18.8 (this study was made prior to the banning of leaded fuels). Finer lead particulates are more widely dispersed in the atmosphere and contribute to the general contamination that occurs in cities. Not surprisingly, studies have shown some effects of lead on urban wildlife. For example, pigeons (Columba livia) living in cities can have significant residues of lead and may exhibit symptoms of acute poisoning.

Figure 18.9. Lead Pollution and Vehicular Traffic. Soil was collected near roads of different traffic density in Halifax, and was analyzed for its lead content. Metal data are in ppm dry weight, while average daily traffic (ADT) is in vehicles per day. The background concentration in soil is 14 ppm. Source: Data from Dale and Freedman (1982).

Overall, there have been large reductions in the emissions of lead in Canada, and also in other developed countries (Figure 18.9). This improvement in environmental conditions has occurred because of the banning of leaded gasoline as well as improved emissions controls at smelters and other industrial facilities.

Figure 18.10. Lead Emissions in Canada. The especially large decrease in 1995 was due to the banning of leaded gasoline, and much of the continuing reduction was due to improvements of industrial practices. Source: Data from Environment Canada (2015).

Conclusions

All of the naturally occurring elements are present in at least a trace level of contamination in all components of the environment – in the air, water, soil, and organisms. Sometimes their concentration is naturally elevated, as occurs when an ore body is present at the surface of the ground. Increasingly, however, anthropogenic activities are responsible for large emissions of toxic elements to the environment, and in some cases this has resulted in serious damage to ecosystems and in toxicity to people. The worst cases of pollution involve industrial practices that are no longer allowed in Canada or other wealthy countries, such as uncontrolled emissions of metals from smelters, the dumping of mercury into aquatic environments, the use of leaded gasoline, and the use of lead shot for hunting. Nevertheless, pollution by toxic elements is still an important problem. Damage is still being caused to ecosystems and organisms by releases of lead, mercury, and other toxic elements. This is true of all parts of the world, although pollution by toxic elements in poorer countries is much less controlled than in wealthier ones.

Questions for Review

1. How can we identify normal (or reference) levels, contamination, and pollution by metals and other elements given that these substances are ubiquitous in the environment?
2. What are the important sources of metal emissions to the environment?
3. What is the difference between the total and available concentrations of metals?
4. Describe the spatial pattern of metal pollution around a large point source of emissions, such as a smelter.

Questions for Discussion

1. Do you think that environmental damage similar to that near Sudbury is likely to be caused if a new smelter is constructed to process the ore mined at the ore deposit at Voisey’s Bay, Labrador? (Note that the ores in both cases are similar – they contain sulphide minerals of nickel and copper.)
2. Important environmental benefits have been gained by banning the use of leaded gasoline in Canada. Why were there long delays in taking similarly vigorous actions against the use of lead shot in hunting and skeet shooting and lead weights in fishing?
3. Pick an element that was examined in this chapter and research its benefits, toxicity, effects on the environment, control, and mitigation.
4. Explain the principles of bioaccumulation and biomagnification using the case of methylmercury in aquatic ecosystems. Why do you think these phenomena were unanticipated “surprises” to environmental scientists?

Exploring Issues

1. Assume that Canada and the United States are negotiating a treaty to govern their emissions of mercury to the environment. You are a science advisor to the Canadian team. Some members of the team want to press for a “zero emissions” policy, believing that no emissions of mercury to the environment are acceptable. They ask for your advice on this issue. What kinds of information about the toxicity of mercury, to humans and to wild ecosystems, do you need in order to give the team objective advice about the proposed zero-emissions policy? Also, is it physically possible to have zero emissions?

References Cited and Further Reading

Allen, H.E., A.W. Garrison, and G.W. Luther III. 1998. Metals in Surface Waters. Ann Arbor Press, Chelsea, MI.

Allen, J. and A. Voiland. 2014. Dam breach at Mount Polley mine in British Columbia. NASA (Visible Earth). http://visibleearth.nasa.gov/view.php?id=84202 Retrieved January, 2015.

Alloway, B.J. (ed.). 2012. Heavy Metals in Soils: Trace Metals and Metalloids in Soils and their Bioavailability. 3rd ed. Springer, New York, NY.

Armstrong, F.A.J. 1979. Mercury in the aquatic environment. Pp. 84-100 in: Effects of Mercury in the Canadian Environment. NRCC No. 16739, National Research Council of Canada, Ottawa, ON.

Bowen, H.J.M. 1979. Environmental Chemistry of the Elements. Academic Press, New York, NY.

Bradshaw, A.D. and M.J. Chadwick. 1981. The Restoration of Land. Blackwell, Oxford, UK. Cox, R.M. and T.C. Hutchinson. 1979. Metal co-tolerances in the grass Deschampsia caespitosa. Nature, 279: 231-233.

Dale, J.M. and B. Freedman. 1982. Lead and zinc contamination of roadside soil and vegetation in Halifax, Nova Scotia. Proceedings of the Nova Scotian Institute of Science, 32: 327-336. http://hdl.handle.net/10222/14063

Environment Canada. 2015. National Pollutant Release Inventory. https://www.ec.gc.ca/inrp-npri/default.asp?lang=En&n=4A577BB9-1

Fimreite, N., R.W. Feif, and J.A. Keith. 1970. Mercury contamination of Canadian prairie seed eaters and their avian predators. Canadian Field-Naturalist, 84: 269-276.

Foulkes, E.C. (ed.). 1990. Biological Effects of Heavy Metals. CRC Press, Boca Raton, FL.

Frank, R., H.E. Braun, K. Ishida, and P. Suda. 1976. Persistent organic and inorganic pesticide residues in orchard soils and vineyards of southern Ontario. Canadian Journal of Soil Science, 56: 463-484.

Freedman, B. 1995. Environmental Ecology. 2nd ed. Academic Press, San Diego, CA.

Freedman, B. and T.C. Hutchinson. 1980. Pollutant inputs from the atmosphere and accumulations in soils and vegetation near a nickel-copper smelter at Sudbury, Ontario, Canada. Canadian Journal of Botany, 58: 108-132.

Gilmour, C.C. and E.A. Henry. 1991. Mercury methylation in aquatic systems affected by acid deposition. Environmental Pollution, 71: 131-169.

Gunn, J.M. (ed.). 1995. Restoration and Recovery of an Industrial Region: Progress in Restoring the Smelter-Damaged Landscape near Sudbury, Canada. Springer, New York, NY.

Harada, M. 2001. Minamata disease and the mercury pollution of the globe. Environmental Information Network for Asia and the Pacific. http://www.einap.org/envdis/Minamata.html

Johnels, A., G. Tyler, and T. Westermark. 1979. A history of mercury levels in Swedish fauna. Ambio, 8: 160-168.

Kruckeberg, A.R. 1984. California Serpentine: Flora, Vegetation, Geology, Soils, and Management Problems. University of California Press, Los Angeles, CA.

Kuja, A.L. 1980. Revegetation of Mine Tailings using Native Species from Disturbed Sites in Northern Canada. M.Sc. Thesis, Department of Botany, University of Toronto, Toronto, ON.

McKay, C. 1985. Freshwater Fish Contamination in Canadian Waters. Chemical Hazards Division, Department of Fisheries and Oceans, Ottawa, ON.

Mierle, G. 1990. Aqueous inputs of mercury to Precambrian Shield lakes in Ontario. Environmental Contamination & Chemistry, 9: 843-851.

National Aeronautics and Space Agency. 2014. Dam Breach at Mount Polley Mine in British Columbia, August 17, 2014. NASA Earth Observatory. http://earthobservatory.nasa.gov/IOTD/view.php?id=84202&src=ve

Ontario Ministry of Environment and Energy (MOEE). 2014. Eating Ontario Sport Fish (2013-14). MOEE, Toronto, ON. https://web.archive.org/web/20141009013225/http://www.ontario.ca/environment-and-energy/guide-eating-ontario-sport-fish

Peters, T.H. 1984. Rehabilitation of mine tailings: a case of complete ecosystem reconstruction and revegetation of industrially stressed lands in the Sudbury area, Ontario, Canada. Pp. 403-421 In: Effects of Pollutants at the Ecosystem Level. (P.J. Sheehan, D.R. Miller, and P. Bourdeau, eds.), Wiley, New York, NY.

Ripley, E.A., R.E. Redmann, and A.A. Crowder. 1996. Environmental Effects of Mining. St. Lucie Press, Delray Beach, FL.

Salomons, W., U. Förstner, and P. Mader (eds.). 1995. Heavy Metals: Problems and Solutions. Springer, New York, NY.

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Sarkar, B. (ed.). 2002. Heavy Metals in the Environment. Marcel Dekker, New York, NY. Scheuhammer, A.M. and S.L. Norris. 1996. The ecotoxicology of lead shot and lead fishing weights. Ecotoxicology, 5: 279-295.

Spitz, K. and J. Trudinger. 2008. Mining and the Environment: From Ore to Metal. CRC Press, Boca Raton, FL.

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Wang, L.K., J.P. Chen, Y.-T. Hung, and N.K. Shammas. 2009. Heavy Metals in the Environment. CRC Press, Boca Raton, FL.

Wong, M.H.W. and A.D. Bradshaw. 2003. The Restoration and Management of Derelict Land: Modern Approaches. World Scientific Publishers, London, UK.