- Email: [email protected]
Ecotoxicology
Ecotoxicology DW Connell, Griffith University, Nathan, QLD, Australia Ó 2014 Elsevier Inc. All rights reserved. This article is a revision of the previous edition article by F. Moriarty, D.W. Connell, volume 3, pp. 565–572, Ó 1997, Elsevier Inc.
Glossary Bioaccumulation Increase of pollutant concentration in an organism from that in the ambient environment, taking into account the intake from all sources. Chemical speciation Occurrence of well-defined chemical entities such as ions, molecules, and complexes; of particular relevance for heavy metals and some air pollutants. Community structure Numbers and types of species of animals and plants in a distinct system. Dose–response relationship The relationship between the dose and the adverse response exhibited by the organism. Ecosystem Assemblage of species that forms a distinct system (e.g., the species in a lake) and its habitat (e.g., the rocks, sediments, and water in a lake).
Introduction The number of chemicals in commercial use by human society is enormous. Around 70 000 chemicals are commonly utilized for a wide variety of purposes, and the rate of introduction of new substances is in the order of 200–1000 compounds each year (Connell et al., 1999a,b). In recent years there has been a rapid development in industrial technology together with communications and transport which has lead to the development and usage of various chemicals to facilitate these applications. For example metal use in electrical technology has increased substantially, with lithium, mercury, and cadmium in particular being used in increasing quantities as well as a variety of other metals. In addition many totally new compounds have been extensively used for various industrial purposes. An example are the polychlorinated biphenyls (PCBs), which were first introduced in 1929 and used principally as dielectric (insulating) fluids in the electrical industry. Refrigeration and air conditioning systems made extensive use of chlorofluorocarbons. Since the 1960s, a wide range of new plastics have been introduced into packaging and automobile manufacture and many of these substances have become environmental pollutants (Connell, 2005). A landmark in environmental contamination occurred in 1962 when Rachael Carson published her book Silent Spring (Carson, 1962). This revealed for the first time to the general public how trace environmental contaminants were having adverse effects on the natural environment. The study of toxic substances dates from ancient times starting with the search for remedies and cures for ills and
Reference Module in Biomedical Research, 3rd edition
Ecotoxicants Substances which have toxic and detrimental effects on ecosystems. Environment All an organism’s surroundings, both the habitat and the other plants and animals, including other members of its own species. Habitat Inanimate, or abiotic, components of the environment for an individual, population, community, or ecosystem. Pollutant Substance that occurs in the environment at least in part as a result of human activities and that has a deleterious effect on living organisms. Population Group of individuals of the same species that are within a defined area or, alternatively, that have the possibility of mating with each other provided the needs are met for opposite sexes and maturity.
marks the start of toxicology. This approach has been used to evaluate toxic effects principally of toxicants such as pharmaceutical chemicals to ensure their safe and effective use. However the broad range of toxicants which are now relatively common in our society includes some toxic substances which can be referred to as ecotoxicants (Connell, 2005). These substances are defined primarily by their manufacture, usage, and disposal, which lead to distribution in the natural environment and the exposure of natural ecosystems to them. They could be discharges from industry (petroleum hydrocarbons, heavy metals, acids, alkalis, solvents), agriculture (herbicides, insecticides), domestic activities (pesticides, petroleum), or other activities which result in discharges to the environment. These ecotoxicants are basically different in chemical nature, behavior, and adverse biological effects to the traditional pharmaceutical chemicals used in treating adverse effects and diseases in the human population but at the same time are also toxicants. The investigation of the ecological impacts of toxic pollutants on ecosystems has required a new approach to toxicology. This approach is described as ecotoxicology (Moriarty, 1988; Walker et al., 2012; Newman, 2009) which must be multidisciplinary, combining the sciences of chemistry, toxicology, and ecology to achieve a satisfactory understanding of the complex interactions with the natural environment involved. In addition there is a managerial aspect, with an increasing need to regulate chemicals to protect human health and the natural environment. Ecotoxicology has been described by Moriarty (1988), as a branch of science which has the role of assessing, monitoring, and predicting the fate of foreign substances in the environment.
http://dx.doi.org/10.1016/B978-0-12-801238-3.00213-0
1
2
Ecotoxicology
The Ecotoxicology Concept Scientific investigations of the effects of environmental pollutants on ecosystems have tended to focus on laboratory investigations of the effects of specific chemicals on individual biological species within broad groups such as fish, crustacea, and zooplankton. The outcomes of these investigations, usually in aquarium tanks in the laboratory, are toxicological measures such as LC50 (toxic concentration to 50% of the test organisms), EC50 (effective concentration to produce a toxic effect with 50% of the test organisms), NOAEL (No Observable Adverse Effect Level), and LOAEL (Lowest Observable Adverse Effect Level). While these values are useful they can only give suggestions as to the likely effects on the complex ecosystems
existing in the natural environment. These systems consist of primary producers, consumers, and predators and involve flows of energy and nutrients, food selection, predator prey relationships, and so on. The effects of pollutants on these ecosystems are of primary management concern and so there is an interest in developing an approach which can accommodate this requirement. The ecotoxicology of a chemical (Connell, 2005) can be seen to be based on a sequence of interactions and effects controlled by the physical, physicochemical, and biological properties of a chemical as indicated in Figure 1. In the first stage after discharge the physical properties of the contaminant, whether it is a solid, liquid, or gas, have a major influence on its dispersal from the source. When the contaminant is physically
Figure 1 Illustration of the ecotoxicology of a chemical with an ecosystem indicating the properties of the chemical and the ecosystem properties involved.
Ecotoxicology
dispersed in the environment, its physicochemical properties, such as aqueous solubility and vapor pressure, influence diffusive movement into different environmental phases leading to environmental levels in water, sediments, and other phases. Environmental levels in these phases results in exposure and uptake by organisms. As the contaminant is now within the organism there can be interactions with the organism at the biochemical, molecular, and cellular level which can lead to lethal and sublethal conditions such as lethal toxicity, reduced reproduction, and so on. These effects on individuals have subsequent influences on populations, communities, and ecosystems which can result in altered species diversity, population structure, and community structure. At latter stages the effects of the chemical enter more complex levels of biological organization, such as the whole ecosystem, and the direct effects of the chemical on individuals become less significant. Thus the biological effects generated at simpler levels of biological organization flow through the system to impact on whole ecosystems rather than the direct toxic effects of the chemical itself at this level of organization.
Types of Ecotoxicant All substances which are discharged to the environment and have a potential impact on ecosystems can be included in this group. Substances which are already present in the environment, but also occur in discharges and add to the environmental occurrence, are in this group. This can lead to the environmental occurrence of abnormally elevated levels and consequent detrimental effects. For example, many metals and related elements occur naturally in the environment in significant concentrations. Lead, arsenic, mercury, and many other substances occur in the oceans, soils, and other parts of the environment and can be elevated due to discharges. For example, excess concentrations of lead occur in the soil of most of the world cities due to the use of leaded motor fuel. Polycyclic aromatic hydrocarbons produced by combustion are present in low concentrations as a natural product of combustion in the environment but levels may have been increased by the expanded usage of fuels leading to discharge and deposition of elevated concentrations in the environment. Thus with many substances which can be considered to be ecotoxicants, there already exists background concentrations within the environment in general with elevated concentrations in specific sectors (Carlow, 1994).
Table 1
In addition to the ecotoxicants mentioned above, there are a wide range of synthetic compounds distributed or used in the environment for a variety of purposes. For example, chemicals such as chlorpyrifos, dichloro-diphenyl-trichloro ethane (DDT), and other chlorohydrocarbons, glyphosate, 2,4-dichlorophenoxyacetic acid (2,4-D), and so on are totally new to the environment since they are produced by synthetic chemistry processes in industry. Industrial chemicals such as the chlorobenzenes and most solvents are used and can be distributed to the environment during manufacture, use, accidental spillage, or disposal after use. The organotin compounds, e.g., tributyltin, are applied to the hulls of ships as an antifouling compound and as a result are distributed in the marine environment (Connell, 2005).
Sources of Ecotoxicants Ecotoxicants can originate from most activities of human society and can affect numerous different types of environment as shown in Table 1. It is noteworthy that sewerage is often considered in terms of its biochemical oxygen demand and capability to reduce the dissolved oxygen in receiving water as well as the presence of nitrogen and phosphorus which can cause eutrophication in aquatic areas. But sewerage, in addition to these substances, usually contains a broad range of ecotoxicants at low concentrations (Connell, 2005). The volume of sewerage is relatively high and so the total amount of toxicant discharged to the environment can be relatively large. Discharges due to the operations of oil fields, spillages, and so on are high profile events but in fact sewerage is a major source of petroleum hydrocarbons to the oceans. Industrial discharges to the sewage system are the major sources of these trace toxicants in sewage. However human waste discharges to the sewage system can contain a wide variety of pharmaceuticals and related substances such as steroid hormones, bisphenol A, and many other substances. These are suspected to have endocrinedisrupting activity which has been shown to interfere with reproduction in natural systems with DDE (Walker et al., 2012). Similarly, stormwater also contains a wide array of ecotoxicants in low concentrations. These substances, principally originate from discharges from motor vehicles which are deposited on the road surface and subsequently swept into stormwater. Motor vehicles are a major source of lead and other metals, polycyclic aromatic hydrocarbons, and toxic gasses. All these substances are discharged into the atmosphere which
Sources and types of ecotoxicants discharged to the environment
Source
Some chemical groups involved
Motor vehicle exhausts, electricity generation, and industrial discharges to the atmosphere Sewage
Lead and other toxic metals, carbon monoxide, carbon dioxide, aromatic hydrocarbons, sulfur dioxide, hydro carbons, PCDD, PCDF, PCBsa Aromatic hydrocarbons, hydrocarbons, chlorohydrocarbons, toxic metals, surfactants, pharmaceuticals Aromatic hydrocarbons, hydrocarbons, lead, and other toxic metals Acids, toxic metals, salts, hydrocarbons, PCDDs and PCDFs Toxic metals, salts, hydrocarbons, PCDDs, PCDFs, PCBsa Chlorohydrocarbons, organophosphorus compounds
Stormwater runoff Industrial discharges to waterways Urban and industrial discharges to soil Rural industries a
3
Polychlorodibenzodioxins (PCDDs), polychlorodibenzofurans (PCDFs) and polychlorobiphenyls (PCBs).
4
Ecotoxicology
may have effects on terrestrial systems and human health but many of the toxic compounds are in particulate form and can deposit into soils and the road surface. Thus soils in urban areas can contain significant amounts of lead, polycyclic aromatic hydrocarbons, and other ecotoxicants which have implications for the natural environment and human health (Connell, 2005). Often, particularly in the past, industrial wastes were disposed of directly into pits dug into soil and so the soil can be contaminated and possibly the ground water as well. Outside urban and industrial areas mining and agricultural activities are probably the major sources of contaminants. These are discharged principally to waterways, the atmosphere, and soil. Growth of crops in agriculture often involves the widespread use of pesticides including insecticides and herbicides which can contaminate soil. The transport of these toxicants in storm water runoff into adjacent waterways causes water pollution. In addition terrestrial ecosystems can be contaminated resulting in adverse effects on animals and plants. The accidental spillage of petroleum is perhaps the most spectacular example of toxicant contamination of the environment. Components of the petroleum, such as the toxic aromatic hydrocarbons, can dissolve in water and have adverse effects on aquatic organisms. The immediate effects can be large-scale lethalities to many different types of organism but long-term sublethal effects may occur and recovery can be slow. The contaminant concentrations are reduced by environmental processes such as evaporation and the contaminants can be chemically transformed by processes such as oxidation.
Figure 2 Conceptualization of the transfer processes involved in the movement of a toxicant from the environment to the site of action.
Mode of Action and Toxic Effects on Individuals Toxicants distribute in the environment by a variety of processes so that various levels can occur in the water, air, soil, or food as a result of direct discharges, transport from elsewhere, or biotransformation of another substance. This is the initial process in the ecotoxicology concept of the interaction of chemicals with ecosystems as shown in Figure 1. A toxic effect on an individual organism occurs when the toxicant, or a derived active substance, is transferred to the site of action within the organism by the processes generalized in Figure 2. The toxic chemical is taken up by the organism through the stomach, gills, lungs, etc. and then distributed by the circulatory fluid throughout the body, where it may be biotransformed and excreted. Some of the original compound, or its biotransformed active product, may be transferred to the site of action. With lipophilic compounds, such as DDT, dieldrin, PCBs, and so on, the site of action is the lipoid tissue in the organism and the compound is transferred to this site by the circulatory fluid often blood. Chlorpyrifos, an organophosphate pesticide, is a neurotoxicant and inhibits nerve impulses through inhibition of the enzyme, acetylcholinesterase within the nerves which are the sites of action. Chemicals can be classed as toxicants if they have a toxic effect on biota. In addition toxicants can be divided into different groups based on various factors: for example, the type of deleterious biological effect they exert, the broad type of biological group affected, the broad chemical class to which they belong, or the physicochemical property that dominates their toxic action (Connell, 2005). Some toxicants are
identified by the biological groups affected; for example, insecticides are chemicals which are toxic to insects, whereas weedicides are toxic to weeds. Other chemicals are classified by their toxic effect: for example, carcinogens for cancer-causing chemicals and so on. The term dose, taken from pharmacology, indicates the intake of a pollutant by an organism from its exposure. In general terms, there are two routes by which animals can acquire pollutants: by ingestion with their food and from direct contact with their inanimate environment, across the body surfaces in general or the respiratory surfaces in particular. For most plants, direct contact is the only route – with the air or the soil. There are also two mechanisms by which organisms can lose pollutants (Figure 2) by excretion and by metabolism, when the pollutant is converted into one or more other compounds within the organism. With a constant exposure, the amount of pollutant within the organism tends to approach a steady state when the rate of intake equals the sum of the rates of excretion and metabolism. Pollutants are not distributed uniformly within organisms. Compartmental models have been developed to describe amounts of pollutant within organisms during and after exposure. For aquatic animals exposed to organic compounds, a much simpler approach is commonly used. Evidence suggests, at least for many pollutants, that food is not a significant route of intake. For many organic compounds, the degree of bioconcentration increases with the n-octanol:water partition coefficient (commonly denoted as P or KOW). The degree of bioconcentration depends on the distribution ratio of the
Ecotoxicology
5
their absence. At increased concentrations the effects become less harmful, i.e., first irreversible and then reversible effects occur, until the toxicant is present at a concentration range suitable for normal metabolism (C1 to C2), at which no deleterious effects are exerted. As the concentration of an essential substance increases beyond this range (>C2), toxic effects become apparent and become increasingly deleterious, leading eventually to death. With a toxicant which is nonessential the biological response curve is represented by Curve 2 in Figure 3 which indicates increasing toxic effects at increasing doses.
Effects of Toxicants on Natural Populations Figure 3 Conceptual responses of biota to concentrations of a toxicant which is an essential chemical to growth but becomes toxic at relatively high concentrations (1) and a chemical which is nonessential to growth (2).
compound between the ambient water and the animal’s fats, which is indicated by the bioconcentration factor (KB concentration in organism/concentration in water). Terrestrial animals will often acquire most of their pollutant burden from their food. The relation between concentrations of pollutant in predator and prey depends on many factors, but it is doubtful that persistent pollutants inevitably increase in concentration along food chains. Intake often depends on the specific details of the exposure: the distribution and chemical form of the pollutant within the air, soil water, or sediment. For most chemicals, there are relationships between the biological effect observed and either the toxicant concentration in the ambient environment (e.g., water with fish) or dose (e.g., occurrence of lead in food with humans). These relationships are collectively termed dose–response relationships. An aspect of environmental toxicology that is of particular importance is that some environmental toxicants are in fact essential to growth and development at low concentrations, but become toxic at higher concentrations. These substances are mainly metals such as iron, magnesium, zinc, copper, and a variety of other substances. The general nature of the relationship between dose (or concentration) and biological response is different for chemicals essential to the organism’s metabolism and those that are nonessential (as illustrated in Figure 3). For essential substances, the relationship is parabolic – see Curve 1 in Figure 3. When present at concentrations (
Table 2
Individuals of particular species occur as populations within an ecosystem. But instead of individuals of a particular species with a common size, age, and so on, as used in laboratory testing of organisms, the population has individuals of different life stages, ages, size, etc. as they occur in the natural system. Thus chemical exposure with natural populations gives rise to a variety of possible responses. These responses depend not only the nature of the chemical but the dose and period of exposure that occurs. A generalized sequence of the effects of a chemical on a population is shown in Table 2. At very high and very high doses the exposure period, of the order of hours, is short and death is the common response. At intermediate doses a major proportion of the population survives, but survivors can exhibit severe effects in many cases. The lethal doses (dose and concentration) at intermediate levels causes about equal numbers of deaths and survivors but the survivors can have severe sublethal effects. At low to very low doses the exposure period can be very long of the order of years or a life time. There can be the death of the sensitive individuals in the population or there may be no observable effects at all. In most environmental systems the exposure can be low to very low and conventional biological techniques are unable to detect any effects. An effect that has been recently proposed for these situations is the reduced life expectancy (Connell and Yu, 2009). This concept evaluates the overall impact of chemicals on organisms as a reduction in the life expectancy from that which would be expected in unexposed organisms. Overall these effects on natural populations can lead to changes in the structure of the population from the normal to one in which the sensitive individuals have been removed by the chemical stress. With aquatic population this could be the lowering of the population of fish eggs and fry as these are usually the most sensitive members of the population.
Generalized effects of toxicants at different doses and exposure times on ecosystems
Increasing doseY
[Increasing exposure period
Dose
Exposure period
Response
Very low Low
Very long (many years) Long (months year 1)
l
Intermediate
Intermediate (days)
High Very high
Short (hours per day) Very short (hours)
l l l l l l
No detectable effects Death of sensitive individuals Sublethal effects in survivors Equal numbers of deaths and survivors Severe effects in some survivors Few resistant individuals survive Death to all members of the population
6
Ecotoxicology
Some General Effects of Toxicants on Ecosystems In addressing the toxic effects on ecosystems, attention has been given to the direct investigation of the effects of toxicants on test sections of large natural ecosystems (mesocosms) and small artificial simplified ecosystems (microcosms). Some general principles have emerged which can be of assistance in interpreting the effects of chemicals on ecosystems. Within most ecosystems there are many different species. Some within the primary producers, consumers, and predators which can fall into the various biological classifications. But a basic principle, irrespective of biological classification, is that the species of organisms in an ecosystem exhibit differing susceptibilities to toxicants. For example, herbicides that are selectively toxic to plants and insecticides have a major impact on insect populations. Within these broad groups of species there are wide ranges of different susceptibilities with different individual species with some species being very susceptible to a given toxicant and other species being very resistant. Thus, when any toxicant enters an ecosystem it will selectively remove those susceptible species from the range of organisms present. This generally translates into a reduction in the species number and diversity of organisms present and a change in the community structure. In addition to direct toxic effects on different component species in an ecosystem, other important secondary effects usually result. In an ecosystem there are a wide range of interacting and interdependent organisms including microorganisms, plants, invertebrates, vertebrates, and so on. In many cases the effects due to a toxicant are large compared with natural variations and can lead to more obvious ecological effects. Selective removal or alteration of a population of organisms in an ecosystem can result in modification of the food web. This then results in a change in energy and matter flow patterns. In an ecosystem characteristics such as total respiration, total primary production, respiration to primary production ratio, nutrient cycling rates, predator–prey relationships, and so on are often changed.
Management of Chemicals The Organisation for Economic Co-operation and Development (OECD) has made considerable efforts to develop and harmonize the tests required by different countries when assessing new chemicals. The details can vary considerably between countries, but there is widespread agreement on the rationale. This is to estimate amounts released, environmental distribution, and concentration and to compare the predicted environmental concentrations with those needed to affect organisms. This is applying the ecotoxicological approach previously described (see Figure 1). The assessment of new chemicals requires the application of a set of laboratory tests. These tests of biological effects usually include tests of the exposure needed to produce adverse effects on a range of species, which usually include fish and crustacea, and can include, particularly for pesticides, birds, bees, other beneficial insects, and earthworms. Tests on bioaccumulation are commonly required, usually with a species of fish, but the details vary with intended uses of the chemical, quantities
involved, and the results of earlier tests. Testing is performed by the manufacturer or supplier and continues until either a decision about permitted uses, if any, is made or the manufacturer withdraws the application. This procedure takes little account of possible interactions that may occur between the chemical being considered and other pollutants that may also be present in the environment. Sometimes the observed effect is greater than the sum of the individual effects of exposure to the contaminants alone or it can be less. The degree of effect of a pollutant can depend on the presence or absence of another pollutant. More information is required before we can decide whether pollutants affect each other’s biological activity.
Monitoring Ecotoxicological Effects Present abilities to understand and predict the pathways that pollutants follow in the environment and the effects that they exert are inadequate. We need, therefore, to make repeated surveys (surveillance), or what is usually called monitoring. Three types of information may be sought: 1. rates of release of pollutants into the environment; 2. degree and changes of environmental contamination; and 3. biological effects. Whatever the purpose of a monitoring scheme is, it is essential that objectives are determined at the start because the objectives dictate the details of the sampling program. It is also desirable that it should be known what specified degree of change can be detected with an appropriate degree of statistical significance. Many monitoring schemes do not meet these criteria. Measurements of concentrations of a pollutant in nonliving samples or in organisms can be related to standards (i.e., acceptable limits of contamination). Organisms can have advantages over nonliving samples since they acquire much higher concentrations of some pollutants, making chemical analysis easier. They also give a measure of the pollutant’s availability, which is more relevant for the probability of biological effects than is a measure of the amount in the abiotic environment. A recent development is the establishment of environmental specimen banks, collections taken from both living and inanimate components of our environment for indefinite storage. These samples are being stored in anticipation of future, as yet unforeseen, needs. It must be accepted in relation to specimen banks, as well as current chemical monitoring programs, that although it is often easier to monitor amounts of pollutant rather than their biological effects.
Conclusions The investigation and prediction of the effects of chemicals on natural ecosystems has become a new branch of science described as ecotoxicology. This is a systematic sequential approach which follows the fate, interactions, and ecological effects of a chemical on an ecosystem. It initially addresses the distribution of the chemical in the different sectors of the
Ecotoxicology
abiotic environment following discharge. Models to predict this process are well developed and a quantitative result can be obtained. This result can then be interpreted as the resultant adverse effects on individual organisms in the ecosystem. Later stages in the ecotoxicology process involve the evaluation of the effects of the adverse effects on individuals in populations and whole ecosystems. However, with these later stages in this process, quantitative interpretations are not possible and in most situations only qualitative interpretations are possible.
See also: Mechanisms of Toxicity; Principles of Toxicology; Toxicology of Metals; Toxicology of Persistent Organic Pollutants; Toxicology of Pesticides.
7
Connell, D.W., 2005. Basic Concepts of Environmental Chemistry. Taylor and Francis, Boca Raton, FL. Connell, D.W., Yu, J., 2009. Use of exposure time and life expectancy in models for toxicity to aquatic organisms. Marine Pollution Bulletin 57, 245–249. Connell, D.W., Lam, P., Richardson, B., Wu, R., 1999a. Introduction to Ecotoxicology. Blackwell Science, Oxford, p. 13. Connell, D.W., Lam, P., Richardson, B., Wu, R., 1999b. Introduction to Ecotoxicology. Blackwell Science, Oxford, p. 19. Moriarty, F., 1988. Ecotoxicology, the Study of Pollutants in Ecosystems, second ed. Academic Press, London. Newman, M.C., 2009. Fundamentals of Ecotoxicology, third ed. CRC Press, Boca Raton. Walker, C.H., Hopkin, S.P., Sibly, R.M., Peakall, D.B., 2012. Principles of Ecotoxicology, fourth ed. CRC Press, Boca Raton.
Relevant Websites References Carlow, P., 1994. Handbook of Ecotoxicology. Blackwell Science, Oxford. Carson, R., 1962. Silent Spring. Fawcett Books, New York.
ac.europa.eu/food/plant/protection/evaluation/guidelines/wrkdoc10.en – Guideline Document on Testing in Aquatic Toxicology. www.epa.gov/ecotox/ – US Environment Protection Agency – Policies on Ecotoxicology.
Glossary Bioaccumulation Increase of pollutant concentration in an organism from that in the ambient environment, taking into account the intake from all sources. Chemical speciation Occurrence of well-defined chemical entities such as ions, molecules, and complexes; of particular relevance for heavy metals and some air pollutants. Community structure Numbers and types of species of animals and plants in a distinct system. Dose–response relationship The relationship between the dose and the adverse response exhibited by the organism. Ecosystem Assemblage of species that forms a distinct system (e.g., the species in a lake) and its habitat (e.g., the rocks, sediments, and water in a lake).
Introduction The number of chemicals in commercial use by human society is enormous. Around 70 000 chemicals are commonly utilized for a wide variety of purposes, and the rate of introduction of new substances is in the order of 200–1000 compounds each year (Connell et al., 1999a,b). In recent years there has been a rapid development in industrial technology together with communications and transport which has lead to the development and usage of various chemicals to facilitate these applications. For example metal use in electrical technology has increased substantially, with lithium, mercury, and cadmium in particular being used in increasing quantities as well as a variety of other metals. In addition many totally new compounds have been extensively used for various industrial purposes. An example are the polychlorinated biphenyls (PCBs), which were first introduced in 1929 and used principally as dielectric (insulating) fluids in the electrical industry. Refrigeration and air conditioning systems made extensive use of chlorofluorocarbons. Since the 1960s, a wide range of new plastics have been introduced into packaging and automobile manufacture and many of these substances have become environmental pollutants (Connell, 2005). A landmark in environmental contamination occurred in 1962 when Rachael Carson published her book Silent Spring (Carson, 1962). This revealed for the first time to the general public how trace environmental contaminants were having adverse effects on the natural environment. The study of toxic substances dates from ancient times starting with the search for remedies and cures for ills and
Reference Module in Biomedical Research, 3rd edition
Ecotoxicants Substances which have toxic and detrimental effects on ecosystems. Environment All an organism’s surroundings, both the habitat and the other plants and animals, including other members of its own species. Habitat Inanimate, or abiotic, components of the environment for an individual, population, community, or ecosystem. Pollutant Substance that occurs in the environment at least in part as a result of human activities and that has a deleterious effect on living organisms. Population Group of individuals of the same species that are within a defined area or, alternatively, that have the possibility of mating with each other provided the needs are met for opposite sexes and maturity.
marks the start of toxicology. This approach has been used to evaluate toxic effects principally of toxicants such as pharmaceutical chemicals to ensure their safe and effective use. However the broad range of toxicants which are now relatively common in our society includes some toxic substances which can be referred to as ecotoxicants (Connell, 2005). These substances are defined primarily by their manufacture, usage, and disposal, which lead to distribution in the natural environment and the exposure of natural ecosystems to them. They could be discharges from industry (petroleum hydrocarbons, heavy metals, acids, alkalis, solvents), agriculture (herbicides, insecticides), domestic activities (pesticides, petroleum), or other activities which result in discharges to the environment. These ecotoxicants are basically different in chemical nature, behavior, and adverse biological effects to the traditional pharmaceutical chemicals used in treating adverse effects and diseases in the human population but at the same time are also toxicants. The investigation of the ecological impacts of toxic pollutants on ecosystems has required a new approach to toxicology. This approach is described as ecotoxicology (Moriarty, 1988; Walker et al., 2012; Newman, 2009) which must be multidisciplinary, combining the sciences of chemistry, toxicology, and ecology to achieve a satisfactory understanding of the complex interactions with the natural environment involved. In addition there is a managerial aspect, with an increasing need to regulate chemicals to protect human health and the natural environment. Ecotoxicology has been described by Moriarty (1988), as a branch of science which has the role of assessing, monitoring, and predicting the fate of foreign substances in the environment.
http://dx.doi.org/10.1016/B978-0-12-801238-3.00213-0
1
2
Ecotoxicology
The Ecotoxicology Concept Scientific investigations of the effects of environmental pollutants on ecosystems have tended to focus on laboratory investigations of the effects of specific chemicals on individual biological species within broad groups such as fish, crustacea, and zooplankton. The outcomes of these investigations, usually in aquarium tanks in the laboratory, are toxicological measures such as LC50 (toxic concentration to 50% of the test organisms), EC50 (effective concentration to produce a toxic effect with 50% of the test organisms), NOAEL (No Observable Adverse Effect Level), and LOAEL (Lowest Observable Adverse Effect Level). While these values are useful they can only give suggestions as to the likely effects on the complex ecosystems
existing in the natural environment. These systems consist of primary producers, consumers, and predators and involve flows of energy and nutrients, food selection, predator prey relationships, and so on. The effects of pollutants on these ecosystems are of primary management concern and so there is an interest in developing an approach which can accommodate this requirement. The ecotoxicology of a chemical (Connell, 2005) can be seen to be based on a sequence of interactions and effects controlled by the physical, physicochemical, and biological properties of a chemical as indicated in Figure 1. In the first stage after discharge the physical properties of the contaminant, whether it is a solid, liquid, or gas, have a major influence on its dispersal from the source. When the contaminant is physically
Figure 1 Illustration of the ecotoxicology of a chemical with an ecosystem indicating the properties of the chemical and the ecosystem properties involved.
Ecotoxicology
dispersed in the environment, its physicochemical properties, such as aqueous solubility and vapor pressure, influence diffusive movement into different environmental phases leading to environmental levels in water, sediments, and other phases. Environmental levels in these phases results in exposure and uptake by organisms. As the contaminant is now within the organism there can be interactions with the organism at the biochemical, molecular, and cellular level which can lead to lethal and sublethal conditions such as lethal toxicity, reduced reproduction, and so on. These effects on individuals have subsequent influences on populations, communities, and ecosystems which can result in altered species diversity, population structure, and community structure. At latter stages the effects of the chemical enter more complex levels of biological organization, such as the whole ecosystem, and the direct effects of the chemical on individuals become less significant. Thus the biological effects generated at simpler levels of biological organization flow through the system to impact on whole ecosystems rather than the direct toxic effects of the chemical itself at this level of organization.
Types of Ecotoxicant All substances which are discharged to the environment and have a potential impact on ecosystems can be included in this group. Substances which are already present in the environment, but also occur in discharges and add to the environmental occurrence, are in this group. This can lead to the environmental occurrence of abnormally elevated levels and consequent detrimental effects. For example, many metals and related elements occur naturally in the environment in significant concentrations. Lead, arsenic, mercury, and many other substances occur in the oceans, soils, and other parts of the environment and can be elevated due to discharges. For example, excess concentrations of lead occur in the soil of most of the world cities due to the use of leaded motor fuel. Polycyclic aromatic hydrocarbons produced by combustion are present in low concentrations as a natural product of combustion in the environment but levels may have been increased by the expanded usage of fuels leading to discharge and deposition of elevated concentrations in the environment. Thus with many substances which can be considered to be ecotoxicants, there already exists background concentrations within the environment in general with elevated concentrations in specific sectors (Carlow, 1994).
Table 1
In addition to the ecotoxicants mentioned above, there are a wide range of synthetic compounds distributed or used in the environment for a variety of purposes. For example, chemicals such as chlorpyrifos, dichloro-diphenyl-trichloro ethane (DDT), and other chlorohydrocarbons, glyphosate, 2,4-dichlorophenoxyacetic acid (2,4-D), and so on are totally new to the environment since they are produced by synthetic chemistry processes in industry. Industrial chemicals such as the chlorobenzenes and most solvents are used and can be distributed to the environment during manufacture, use, accidental spillage, or disposal after use. The organotin compounds, e.g., tributyltin, are applied to the hulls of ships as an antifouling compound and as a result are distributed in the marine environment (Connell, 2005).
Sources of Ecotoxicants Ecotoxicants can originate from most activities of human society and can affect numerous different types of environment as shown in Table 1. It is noteworthy that sewerage is often considered in terms of its biochemical oxygen demand and capability to reduce the dissolved oxygen in receiving water as well as the presence of nitrogen and phosphorus which can cause eutrophication in aquatic areas. But sewerage, in addition to these substances, usually contains a broad range of ecotoxicants at low concentrations (Connell, 2005). The volume of sewerage is relatively high and so the total amount of toxicant discharged to the environment can be relatively large. Discharges due to the operations of oil fields, spillages, and so on are high profile events but in fact sewerage is a major source of petroleum hydrocarbons to the oceans. Industrial discharges to the sewage system are the major sources of these trace toxicants in sewage. However human waste discharges to the sewage system can contain a wide variety of pharmaceuticals and related substances such as steroid hormones, bisphenol A, and many other substances. These are suspected to have endocrinedisrupting activity which has been shown to interfere with reproduction in natural systems with DDE (Walker et al., 2012). Similarly, stormwater also contains a wide array of ecotoxicants in low concentrations. These substances, principally originate from discharges from motor vehicles which are deposited on the road surface and subsequently swept into stormwater. Motor vehicles are a major source of lead and other metals, polycyclic aromatic hydrocarbons, and toxic gasses. All these substances are discharged into the atmosphere which
Sources and types of ecotoxicants discharged to the environment
Source
Some chemical groups involved
Motor vehicle exhausts, electricity generation, and industrial discharges to the atmosphere Sewage
Lead and other toxic metals, carbon monoxide, carbon dioxide, aromatic hydrocarbons, sulfur dioxide, hydro carbons, PCDD, PCDF, PCBsa Aromatic hydrocarbons, hydrocarbons, chlorohydrocarbons, toxic metals, surfactants, pharmaceuticals Aromatic hydrocarbons, hydrocarbons, lead, and other toxic metals Acids, toxic metals, salts, hydrocarbons, PCDDs and PCDFs Toxic metals, salts, hydrocarbons, PCDDs, PCDFs, PCBsa Chlorohydrocarbons, organophosphorus compounds
Stormwater runoff Industrial discharges to waterways Urban and industrial discharges to soil Rural industries a
3
Polychlorodibenzodioxins (PCDDs), polychlorodibenzofurans (PCDFs) and polychlorobiphenyls (PCBs).
4
Ecotoxicology
may have effects on terrestrial systems and human health but many of the toxic compounds are in particulate form and can deposit into soils and the road surface. Thus soils in urban areas can contain significant amounts of lead, polycyclic aromatic hydrocarbons, and other ecotoxicants which have implications for the natural environment and human health (Connell, 2005). Often, particularly in the past, industrial wastes were disposed of directly into pits dug into soil and so the soil can be contaminated and possibly the ground water as well. Outside urban and industrial areas mining and agricultural activities are probably the major sources of contaminants. These are discharged principally to waterways, the atmosphere, and soil. Growth of crops in agriculture often involves the widespread use of pesticides including insecticides and herbicides which can contaminate soil. The transport of these toxicants in storm water runoff into adjacent waterways causes water pollution. In addition terrestrial ecosystems can be contaminated resulting in adverse effects on animals and plants. The accidental spillage of petroleum is perhaps the most spectacular example of toxicant contamination of the environment. Components of the petroleum, such as the toxic aromatic hydrocarbons, can dissolve in water and have adverse effects on aquatic organisms. The immediate effects can be large-scale lethalities to many different types of organism but long-term sublethal effects may occur and recovery can be slow. The contaminant concentrations are reduced by environmental processes such as evaporation and the contaminants can be chemically transformed by processes such as oxidation.
Figure 2 Conceptualization of the transfer processes involved in the movement of a toxicant from the environment to the site of action.
Mode of Action and Toxic Effects on Individuals Toxicants distribute in the environment by a variety of processes so that various levels can occur in the water, air, soil, or food as a result of direct discharges, transport from elsewhere, or biotransformation of another substance. This is the initial process in the ecotoxicology concept of the interaction of chemicals with ecosystems as shown in Figure 1. A toxic effect on an individual organism occurs when the toxicant, or a derived active substance, is transferred to the site of action within the organism by the processes generalized in Figure 2. The toxic chemical is taken up by the organism through the stomach, gills, lungs, etc. and then distributed by the circulatory fluid throughout the body, where it may be biotransformed and excreted. Some of the original compound, or its biotransformed active product, may be transferred to the site of action. With lipophilic compounds, such as DDT, dieldrin, PCBs, and so on, the site of action is the lipoid tissue in the organism and the compound is transferred to this site by the circulatory fluid often blood. Chlorpyrifos, an organophosphate pesticide, is a neurotoxicant and inhibits nerve impulses through inhibition of the enzyme, acetylcholinesterase within the nerves which are the sites of action. Chemicals can be classed as toxicants if they have a toxic effect on biota. In addition toxicants can be divided into different groups based on various factors: for example, the type of deleterious biological effect they exert, the broad type of biological group affected, the broad chemical class to which they belong, or the physicochemical property that dominates their toxic action (Connell, 2005). Some toxicants are
identified by the biological groups affected; for example, insecticides are chemicals which are toxic to insects, whereas weedicides are toxic to weeds. Other chemicals are classified by their toxic effect: for example, carcinogens for cancer-causing chemicals and so on. The term dose, taken from pharmacology, indicates the intake of a pollutant by an organism from its exposure. In general terms, there are two routes by which animals can acquire pollutants: by ingestion with their food and from direct contact with their inanimate environment, across the body surfaces in general or the respiratory surfaces in particular. For most plants, direct contact is the only route – with the air or the soil. There are also two mechanisms by which organisms can lose pollutants (Figure 2) by excretion and by metabolism, when the pollutant is converted into one or more other compounds within the organism. With a constant exposure, the amount of pollutant within the organism tends to approach a steady state when the rate of intake equals the sum of the rates of excretion and metabolism. Pollutants are not distributed uniformly within organisms. Compartmental models have been developed to describe amounts of pollutant within organisms during and after exposure. For aquatic animals exposed to organic compounds, a much simpler approach is commonly used. Evidence suggests, at least for many pollutants, that food is not a significant route of intake. For many organic compounds, the degree of bioconcentration increases with the n-octanol:water partition coefficient (commonly denoted as P or KOW). The degree of bioconcentration depends on the distribution ratio of the
Ecotoxicology
5
their absence. At increased concentrations the effects become less harmful, i.e., first irreversible and then reversible effects occur, until the toxicant is present at a concentration range suitable for normal metabolism (C1 to C2), at which no deleterious effects are exerted. As the concentration of an essential substance increases beyond this range (>C2), toxic effects become apparent and become increasingly deleterious, leading eventually to death. With a toxicant which is nonessential the biological response curve is represented by Curve 2 in Figure 3 which indicates increasing toxic effects at increasing doses.
Effects of Toxicants on Natural Populations Figure 3 Conceptual responses of biota to concentrations of a toxicant which is an essential chemical to growth but becomes toxic at relatively high concentrations (1) and a chemical which is nonessential to growth (2).
compound between the ambient water and the animal’s fats, which is indicated by the bioconcentration factor (KB concentration in organism/concentration in water). Terrestrial animals will often acquire most of their pollutant burden from their food. The relation between concentrations of pollutant in predator and prey depends on many factors, but it is doubtful that persistent pollutants inevitably increase in concentration along food chains. Intake often depends on the specific details of the exposure: the distribution and chemical form of the pollutant within the air, soil water, or sediment. For most chemicals, there are relationships between the biological effect observed and either the toxicant concentration in the ambient environment (e.g., water with fish) or dose (e.g., occurrence of lead in food with humans). These relationships are collectively termed dose–response relationships. An aspect of environmental toxicology that is of particular importance is that some environmental toxicants are in fact essential to growth and development at low concentrations, but become toxic at higher concentrations. These substances are mainly metals such as iron, magnesium, zinc, copper, and a variety of other substances. The general nature of the relationship between dose (or concentration) and biological response is different for chemicals essential to the organism’s metabolism and those that are nonessential (as illustrated in Figure 3). For essential substances, the relationship is parabolic – see Curve 1 in Figure 3. When present at concentrations (
Table 2
Individuals of particular species occur as populations within an ecosystem. But instead of individuals of a particular species with a common size, age, and so on, as used in laboratory testing of organisms, the population has individuals of different life stages, ages, size, etc. as they occur in the natural system. Thus chemical exposure with natural populations gives rise to a variety of possible responses. These responses depend not only the nature of the chemical but the dose and period of exposure that occurs. A generalized sequence of the effects of a chemical on a population is shown in Table 2. At very high and very high doses the exposure period, of the order of hours, is short and death is the common response. At intermediate doses a major proportion of the population survives, but survivors can exhibit severe effects in many cases. The lethal doses (dose and concentration) at intermediate levels causes about equal numbers of deaths and survivors but the survivors can have severe sublethal effects. At low to very low doses the exposure period can be very long of the order of years or a life time. There can be the death of the sensitive individuals in the population or there may be no observable effects at all. In most environmental systems the exposure can be low to very low and conventional biological techniques are unable to detect any effects. An effect that has been recently proposed for these situations is the reduced life expectancy (Connell and Yu, 2009). This concept evaluates the overall impact of chemicals on organisms as a reduction in the life expectancy from that which would be expected in unexposed organisms. Overall these effects on natural populations can lead to changes in the structure of the population from the normal to one in which the sensitive individuals have been removed by the chemical stress. With aquatic population this could be the lowering of the population of fish eggs and fry as these are usually the most sensitive members of the population.
Generalized effects of toxicants at different doses and exposure times on ecosystems
Increasing doseY
[Increasing exposure period
Dose
Exposure period
Response
Very low Low
Very long (many years) Long (months year 1)
l
Intermediate
Intermediate (days)
High Very high
Short (hours per day) Very short (hours)
l l l l l l
No detectable effects Death of sensitive individuals Sublethal effects in survivors Equal numbers of deaths and survivors Severe effects in some survivors Few resistant individuals survive Death to all members of the population
6
Ecotoxicology
Some General Effects of Toxicants on Ecosystems In addressing the toxic effects on ecosystems, attention has been given to the direct investigation of the effects of toxicants on test sections of large natural ecosystems (mesocosms) and small artificial simplified ecosystems (microcosms). Some general principles have emerged which can be of assistance in interpreting the effects of chemicals on ecosystems. Within most ecosystems there are many different species. Some within the primary producers, consumers, and predators which can fall into the various biological classifications. But a basic principle, irrespective of biological classification, is that the species of organisms in an ecosystem exhibit differing susceptibilities to toxicants. For example, herbicides that are selectively toxic to plants and insecticides have a major impact on insect populations. Within these broad groups of species there are wide ranges of different susceptibilities with different individual species with some species being very susceptible to a given toxicant and other species being very resistant. Thus, when any toxicant enters an ecosystem it will selectively remove those susceptible species from the range of organisms present. This generally translates into a reduction in the species number and diversity of organisms present and a change in the community structure. In addition to direct toxic effects on different component species in an ecosystem, other important secondary effects usually result. In an ecosystem there are a wide range of interacting and interdependent organisms including microorganisms, plants, invertebrates, vertebrates, and so on. In many cases the effects due to a toxicant are large compared with natural variations and can lead to more obvious ecological effects. Selective removal or alteration of a population of organisms in an ecosystem can result in modification of the food web. This then results in a change in energy and matter flow patterns. In an ecosystem characteristics such as total respiration, total primary production, respiration to primary production ratio, nutrient cycling rates, predator–prey relationships, and so on are often changed.
Management of Chemicals The Organisation for Economic Co-operation and Development (OECD) has made considerable efforts to develop and harmonize the tests required by different countries when assessing new chemicals. The details can vary considerably between countries, but there is widespread agreement on the rationale. This is to estimate amounts released, environmental distribution, and concentration and to compare the predicted environmental concentrations with those needed to affect organisms. This is applying the ecotoxicological approach previously described (see Figure 1). The assessment of new chemicals requires the application of a set of laboratory tests. These tests of biological effects usually include tests of the exposure needed to produce adverse effects on a range of species, which usually include fish and crustacea, and can include, particularly for pesticides, birds, bees, other beneficial insects, and earthworms. Tests on bioaccumulation are commonly required, usually with a species of fish, but the details vary with intended uses of the chemical, quantities
involved, and the results of earlier tests. Testing is performed by the manufacturer or supplier and continues until either a decision about permitted uses, if any, is made or the manufacturer withdraws the application. This procedure takes little account of possible interactions that may occur between the chemical being considered and other pollutants that may also be present in the environment. Sometimes the observed effect is greater than the sum of the individual effects of exposure to the contaminants alone or it can be less. The degree of effect of a pollutant can depend on the presence or absence of another pollutant. More information is required before we can decide whether pollutants affect each other’s biological activity.
Monitoring Ecotoxicological Effects Present abilities to understand and predict the pathways that pollutants follow in the environment and the effects that they exert are inadequate. We need, therefore, to make repeated surveys (surveillance), or what is usually called monitoring. Three types of information may be sought: 1. rates of release of pollutants into the environment; 2. degree and changes of environmental contamination; and 3. biological effects. Whatever the purpose of a monitoring scheme is, it is essential that objectives are determined at the start because the objectives dictate the details of the sampling program. It is also desirable that it should be known what specified degree of change can be detected with an appropriate degree of statistical significance. Many monitoring schemes do not meet these criteria. Measurements of concentrations of a pollutant in nonliving samples or in organisms can be related to standards (i.e., acceptable limits of contamination). Organisms can have advantages over nonliving samples since they acquire much higher concentrations of some pollutants, making chemical analysis easier. They also give a measure of the pollutant’s availability, which is more relevant for the probability of biological effects than is a measure of the amount in the abiotic environment. A recent development is the establishment of environmental specimen banks, collections taken from both living and inanimate components of our environment for indefinite storage. These samples are being stored in anticipation of future, as yet unforeseen, needs. It must be accepted in relation to specimen banks, as well as current chemical monitoring programs, that although it is often easier to monitor amounts of pollutant rather than their biological effects.
Conclusions The investigation and prediction of the effects of chemicals on natural ecosystems has become a new branch of science described as ecotoxicology. This is a systematic sequential approach which follows the fate, interactions, and ecological effects of a chemical on an ecosystem. It initially addresses the distribution of the chemical in the different sectors of the
Ecotoxicology
abiotic environment following discharge. Models to predict this process are well developed and a quantitative result can be obtained. This result can then be interpreted as the resultant adverse effects on individual organisms in the ecosystem. Later stages in the ecotoxicology process involve the evaluation of the effects of the adverse effects on individuals in populations and whole ecosystems. However, with these later stages in this process, quantitative interpretations are not possible and in most situations only qualitative interpretations are possible.
See also: Mechanisms of Toxicity; Principles of Toxicology; Toxicology of Metals; Toxicology of Persistent Organic Pollutants; Toxicology of Pesticides.
7
Connell, D.W., 2005. Basic Concepts of Environmental Chemistry. Taylor and Francis, Boca Raton, FL. Connell, D.W., Yu, J., 2009. Use of exposure time and life expectancy in models for toxicity to aquatic organisms. Marine Pollution Bulletin 57, 245–249. Connell, D.W., Lam, P., Richardson, B., Wu, R., 1999a. Introduction to Ecotoxicology. Blackwell Science, Oxford, p. 13. Connell, D.W., Lam, P., Richardson, B., Wu, R., 1999b. Introduction to Ecotoxicology. Blackwell Science, Oxford, p. 19. Moriarty, F., 1988. Ecotoxicology, the Study of Pollutants in Ecosystems, second ed. Academic Press, London. Newman, M.C., 2009. Fundamentals of Ecotoxicology, third ed. CRC Press, Boca Raton. Walker, C.H., Hopkin, S.P., Sibly, R.M., Peakall, D.B., 2012. Principles of Ecotoxicology, fourth ed. CRC Press, Boca Raton.
Relevant Websites References Carlow, P., 1994. Handbook of Ecotoxicology. Blackwell Science, Oxford. Carson, R., 1962. Silent Spring. Fawcett Books, New York.
ac.europa.eu/food/plant/protection/evaluation/guidelines/wrkdoc10.en – Guideline Document on Testing in Aquatic Toxicology. www.epa.gov/ecotox/ – US Environment Protection Agency – Policies on Ecotoxicology.