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Factors Affecting the Bioavailability of Chemicals
C H A P T E R
6
Factors Affecting the Bioavailability of Chemicals O U T L I N E 6.1 Introduction
66
6.3 Environmental Bioavailability
68
6.2 Pharmacological Bioavailability
66
Relevant Literature and Cited References 71
Abstract
Bioavailability, uptake, metabolism, storage, and excretion of chemicals constitute toxicokinetics. Bioavailability is the potential for uptake of a substance by a living organism. It is usually expressed as the fraction that can be taken up by the organism in relation to the total amount of the substance available. In pharmacology, the bioavailability is the ratio of the amount of a compound in circulation after its extravenous application and its intravenous injection. In aquatic toxicology, environmental bioavailability is usually relevant. Factors affecting the bioavailability of a chemical depend on the route of uptake, and whether the chemical is in the bottom sediment, dissolved in water, or is a constituent of the organisms. In the case of water-soluble substances, the primary source of toxicant is water, and the bioavailability depends on complex formation, especially with humic substances. Even when water-soluble substances are sediment bound, they reside mainly in pore water. Lipid-soluble substances are taken up especially from sediment or from other organisms. The bioavailability from water decreases with increasing lipophilicity and with increasing amount of dissolved organic carbon or colloids in the aquatic phase. With regard to sediment, both the sediment properties (e.g. grain size) and the amount of organic material in the sediment affect bioavailability. The main abiotic factors affecting bioavailability are oxygenation and pH. As an example, metal speciation, affecting bioavailability, depends very much on the pH. Keywords: toxicokinetics; pharmacological bioavailability; absorbed dose fraction; humus; humic acids; fulvic acids; sediment; metal speciation; total organic carbon; dissolved organic carbon; sorption; nanomaterial bioavailability.
An Introduction to Aquatic Toxicology http://dx.doi.org/10.1016/B978-0-12-411574-3.00006-2
65
© 2014 Elsevier Inc. All rights reserved.
66
6. FACTORS AFFECTING THE BIOAVAILABILITY OF CHEMICALS
6.1 INTRODUCTION The bioavailability of a toxicant, its uptake, metabolism (including transformation), storage, and excretion make up toxicokinetics. Toxicokinetics can thus be defined as the characteristics that affect the amounts of chemicals in the organism (Figure 6.1), and these constitute the material for this and the following chapters (Chapters 7, 8, 9, and 10). The first step of toxicokinetics is bioavailability. Bioavailability is the potential for uptake of a substance by a living organism. It is usually expressed as the fraction that can be taken up by an organism in relation to the total amount of the substance available. Notably, it is always the bioavailable fraction of a compound that participates in the uptake and consecutive responses to a chemical, not the total amount. Consequently, a smaller toxicant load in the environment can cause a larger response, if the environment is associated with increased bioavailability (Figure 6.2). Different aspects of bioavailability in the environmental context are given in Figure 6.3. The bioavailability can be divided into pharmacological bioavailability (how the route of administration affects the potential for uptake of a chemical) and environmental bioavailability (how interactions with the environment affect the potential for uptake of a chemical).
6.2 PHARMACOLOGICAL BIOAVAILABILITY In pharmacology, the bioavailability of a compound is mainly determined by the route of administration. The bioavailability of a compound is virtually complete when the route of
FIGURE 6.1 Representation of different components of toxicokinetics as seen in the toxicant level in an organism as a function of time. (A) An organism is exposed to a chemical. Only a portion of the chemical load is bioavailable (total concentration yellow + green, bioavailable fraction green). (B) The chemical is taken up by the organism. The initial uptake rate is a linear function of the bioavailable fraction of the chemical in the environment. However, after a time, the rate of uptake becomes curvilinear, as the chemical that is taken up is metabolized and excreted. (C) After a given (chemical-specific) time, a steady state is reached upon continuous exposure, where the uptake and metabolism/excretion are equal. (D) If exposure to the toxicant ends, its concentration in the organism decreases. The time course of depuration depends on the excretion mechanisms.
6.2 Pharmacological Bioavailability
67
FIGURE 6.2 A hypothetical example showing that although the total concentration of a chemical is higher in environment A than in environment B, the bioavailable fraction in the latter (red line) can be greater than that in the former (green line).
FIGURE 6.3 Bioavailability of chemicals by location in the environment. A chemical can be available for uptake by an organism if it is (A) contained in the sediment—this is the case especially for organic compounds and benthic organisms or organisms with roots in sediment; (B) in water—this is the case for water-soluble compounds such as most metal cations and small anions. Apparently water-bound organic compounds are often associated with dissolved organic matter or colloidal material in the water column. (C) Chemicals can also be available for uptake from food organisms—normally lipid-soluble compounds are bioavailable through ingestion of food such as prey organisms.
administration is intravenous injection, and varies with intraperitoneal injection, administration in food, administration in the respiratory medium, or penetration through the organismal surface. The bioavailability is given in those cases from the ratio of the systemic exposure from extravascular (e.v.) exposure to that following intravenous (i.v.) exposure, as described by the equation:
F = Aev Div /Biv Dev (6.1)
where F (absorbed dose fraction) is a measure of the bioavailability; A and B are the areas under the (plasma) concentration–time curve following e.v. and i.v. administration, respectively; and Dev and Div are the administered e.v. and i.v. doses. This pharmacological definition of bioavailability is important in aquatic toxicology, as in experimental manipulations
68
6. FACTORS AFFECTING THE BIOAVAILABILITY OF CHEMICALS
FIGURE 6.4 Different routes of administration of a chemical leading to differences in toxicity. A hypothetical example of the response to a toxicant given via (1) intravenous injection, (2) intraperitoneal injection, (3) force feeding (gavage), or (4) exposure to the chemical in the natural environment. Although the molar amount of the chemical that the organism is exposed to can be the same, the amount reaching the target structure may be very different because of the factors affecting (pharmacological) bioavailability.
different toxicants can be administered via intravenous/intraperitoneal injections, via gavage (force feeding), or as a part of the normal diet, or the organisms may be exposed to toxicants via water. It should be remembered that whenever intravenous/intraperitoneal/subcutaneous injections are used, the normal uptake of chemicals from the environment (see Chapter 7) is bypassed. Thus, any such studies can give information about the toxic actions of the compound when in the animal, but the findings cannot be considered environmentally relevant as the possibilities and mechanisms of uptake have not been considered (see Figure 6.4 for a schematic representation of differences in toxicity due to different ways of administering the chemical). Factors that affect the appearance of a compound (drug) in the systemic circulation affect its pharmacological bioavailability. Such factors include interactions with other drugs or food components taken concurrently (altering absorption), first-pass metabolism, intestinal motility, chemical degradation of the drug by intestinal microflora, physical properties of the drug (hydrophobicity, pKa, solubility) and its formulation (including the speed and duration of the release of the active ingredient from the encapsulation), whether the formulation is administered to a fed or fasted organism, rate of gastric emptying, circadian differences, age, and gender.
6.3 ENVIRONMENTAL BIOAVAILABILITY There are three major environmental components from which chemicals may enter organisms in the aquatic environment: water, bottom sediment, and other organisms. The importance of these as uptake sources varies depending on the water solubility of the compound. Highly water soluble compounds are preferentially taken up from the aqueous phase. Even if the compounds are largely found in sediment, their location and uptake site will be in the pore water. Lipophilic compounds will be obtained either from sediment or, especially, from food (i.e. other organisms). The deposition history of a compound will also affect its availability. If most of the compound has accumulated to bottom sediments over time, the potential for
6.3 Environmental Bioavailability
69
uptake from these sediments will be highest. Finally, different organisms can have markedly different loads of contaminants depending on their feeding habits, their movements between differently contaminated areas, etc. As an example, a sediment-bound contaminant can be transferred in the food web quite differently in the presence of rooted green plants than in the presence of pelagic unicellular algae. Regardless of the main uptake route of the chemical, the factors affecting bioavailability are essentially the same. They are, first, the complex formation of the toxicant with naturally occurring compounds; second, their lipophilicity; and, third, their resemblance to compounds that are specifically taken up. Naturally, the stability of the compound, which may be different in different compartments of aquatic systems, will also influence how it can be taken up. Strictly speaking, this is not an aspect of bioavailability, but a part of the environmental fate of the toxicant. However, the interactions of the chemical with the environment are an important determinant of the subsequent uptake, and therefore must be mentioned at this point. In the bioavailability of compounds one needs to consider both the water and the sediment properties, and also how other organisms affect the properties of compounds taken up. An important component of such organismic interactions is that microorganisms, in particular, may take up substances and render them inaccessible to other organisms that do not eat the microorganisms. Also, when considering bioavailability, the delivery of compounds from the atmosphere by rainfall (frequency is more important than amount) must be taken into account. The total organic carbon content (TOC) and dissolved organic carbon content (DOC) have intimate association with bioavailability. Largely, this is due to many contaminants forming complexes with the carbon compounds. In aquatic systems the most important complex-forming compounds are humic substances. Humic substances are usually large colloidal molecules with several carboxylic acid and phenolic groups. They are usually divided into two classes: the larger humic acids (molecular weight (MW) > 1000, up to 100,000) and the smaller fulvic acids (MW usually < 1000). Because the humic substances contain carboxylate groups, they are normally acidic with an overall negative charge. In solution they usually behave as biphasic weak acids with a pK value around 4. The humic substances are formed by the breakdown of plant matter, and their exact structure is sitedependent, depending on the plants in the environment. Humic substances can also form a major part of the nutrition of prokaryotes. As the humic substances have an overall negative charge, they can form complexes with positively charged metal ions (and other positively charged compounds). Complex formation is especially pronounced with divalent cations, such as Fe2+, Mg2+, and Ca2+. The bioavailability of metals has been studied very intensively. In addition to complex formation, especially with humus, this is affected by the type of metal compound. For example, sulfide minerals may be encapsulated in quartz or other chemically inert minerals, and despite high total concentrations of metals in sediment containing these minerals they may not be bioavailable and thus their environmental effects may remain small. Consequently, as an example, the type of ore containing the metal affects the toxicity of mining effluents to aquatic systems. If the aquatic environment has reducing conditions, for example if they are hypoxic, metal ions are associated with sulfides, e.g. insoluble FeS is formed. Most metal sulfides are poorly soluble, and consequently quite immobile as long as they remain in a chemically reducing environment. Because of this, their bioavailability is reasonably low. Consequently, oxygenation of the aqueous medium (and the sediment) will affect the bioavailability of
70
6. FACTORS AFFECTING THE BIOAVAILABILITY OF CHEMICALS
metals. The reason why arsenic has become a major pollutant is that it is released from the sulfide-based iron ores when they come into contact with oxygen-containing water. In addition to affecting the fate of metals, oxygenation affects both the properties and stability of organic contaminants. The apparent presence and bioavailability of organic toxicants is different in oxic and anoxic sediments. Another sediment property affecting the bioavailability of organic contaminants is the amount of other organic material in the sediment. Increasing organic material tends to increase the sorption of an organic chemical to the sediment, reducing its availability in the aquatic phase. In general, aquatic bioavailability has close interactions with how compounds are moving between bottom sediments and water, and the final equilibria between the two compartments. Particle size and resulting total surface area available for adsorption are both important factors in adsorption processes in the sediments, and can affect the bioavailability of compounds. Small particles with large surface-area-to-mass ratios allow more adsorption than an equivalent mass of large particles with small surface-area-to-mass ratios. This is most important with regard to nanomaterials. Because of the surface-area-to-mass dependence of bioavailability, the toxicity of nanomaterials can be strongly affected by the size of particles in the formulations. Since the sedimentation of nanomaterials is affected by the way a test is executed, markedly different bioavailabilities and toxicities of nanomaterials have been reported. Reduced adsorption of compounds to sediments can also affect their bioavailability by affecting the dissolved concentration of a compound in the water surrounding the sediment. In the aqueous phase, the bioavailability of organic contaminants depends on their partitioning between the organic phase and water. Lipophilicity is also an important aspect of chemical uptake in organisms, and its determination and main discussion are given in Chapter 7. However, it needs to be pointed out here that, because of the interactions between organic contaminants and other organic materials in water, the bioavailability of organic contaminants from water will decrease with increasing dissolved organic carbon content and increasing amount of colloids in the aquatic phase. Apart from oxygenation, another abiotic factor affecting bioavailability is pH. The effects of pH have been studied especially with regard to the speciation (and solubility) of metals, as exemplified for aluminum in (Figure 6.5). At pH values above neutral, aluminum ions form insoluble compounds; between pH values 5 and 7, the metal exists FIGURE 6.5 Approximate proportions of the different aluminum species (free cations, hydroxides) as a function of pH.
6.3 Environmental Bioavailability
71
largely as soluble hydroxides; and at pH values below 5, it exists largely as toxic free Al3+ ions. Because of the pH effects, the bioavailability of metals and other compounds may be markedly different in bulk water and in the vicinity of (fish) gills, since there is a large pH gradient in the water from the gills to the bulk water. Also, the mode of toxicity of metals and other compounds may be different at different pH values. Again, as an example, aluminum appears to be mainly a respiratory toxicant at intermediary pH values (5–7), largely because it precipitates on gill filaments, increasing the diffusion distance of oxygen. At lower pH values, it appears to be an ionoregulatory toxicant. The hardness of water (essentially its salinity) also affects bioavailability, mostly of ionic compounds. The effect is largely due to a change in the probability of a toxic ion being taken up instead of a nontoxic one in the uptake site. The bioavailability of metals is often calculated using the biotic ligand model (BLM), which seeks to take into account the effects of complex formation, abiotic environmental factors such as pH, and metal interactions (for details, see Chapter 18). Many of these factors vary seasonally and temporally, and most factors are interrelated. Consequently, changing one factor may affect several others. In addition, generally poorly understood biological factors seem to influence bioaccumulation of metals and thereby affect any predictions of their toxicity: an important factor here is the type of aquatic environment. Uptake of ions occurs very differently in marine and freshwater environments. Consequently, what is a useful model in freshwater may not be accurate in the marine environment. The modeling of toxicant accumulation in organisms is discussed further in Chapter 18.
Relevant Literature and Cited References Andrady, A.L., 2011. Microplastics in the marine environment. Mar. Pollut. Bull. 62, 1596–1605. Beckett, R., Jue, Z., Giddings, J.C., 1987. Determination of molecular weight distributions of fulvic and humic acids using flow field–flow fractionation. Environ. Sci. Technol. 21, 289–295. Boudou, A., Ribeyre, F., 1997. Aquatic ecotoxicology: From the ecosystem to the cellular and molecular levels. Environ. Health Perspect. 105 (Suppl. 1), 21–35. Burton Jr., G.A., 2010. Metal bioavailability and toxicity in sediment. Crit. Rev. Environ. Sci. Technol. 40, 852–907. Camargo, J.A., 2003. Fluoride toxicity to aquatic organisms: A review. Chemosphere 50, 251–264. Chapman, P.M., Wang, F., Janssen, C., Persoone, G., Allen, H.E., 1998. Ecotoxicology of metals in aquatic sediments: Binding and release, bioavailability, risk assessment, and remediation. Can. J. Fish Aquat. Sci. 55, 2221–2243. Farrington, J.W., 1991. Biogeochemical processes governing exposure and uptake of organic pollutant compounds in aquatic organisms. Environ. Health Perspect. 90, 75–84. Haitzer, M., Hoss, S., Traunspurger, W., Steinberg, C., 1998. Effects of dissolved organic matter (DOM) on the bioconcentration of organic chemicals in aquatic organisms: A review. Chemosphere 37, 1335–1362. Hamelink, J.L., Landrum, P.F., Bergman, H.L., Benson, W.H., 1994. Bioavailability: Physical, Chemical and Biological Interactions. CRC Press, Boca Raton, FL. Haws, N.W., Ball, W.P., Bouwer, E.J., 2006. Modeling and interpreting bioavailability of organic contaminant mixtures in subsurface environments. J. Contam. Hydrol. 82, 255–292. Henry, T.B., Petersen, E.J., Compton, R.N., 2011. Aqueous fullerene aggregates (nC60) generate minimal reactive oxygen species and are of low toxicity in fish: A revision of previous reports. Curr. Opin. Biotechnol. 22, 533–537. Markich, S.J., 2002. Uranium speciation and bioavailability in aquatic systems: An overview. Sci. World J. 2, 707–729. Navarro, E., Baun, A., Behra, R., Hartmann, N.B., Filser, J., Miao, A.J., Quigg, A., Santschi, P.H., Sigg, L., 2008. Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17, 372–386. Porcal, P., Koprivnjak, J.F., Molot, L.A., Dillon, P.J., 2009. Humic substances—part 7: The biogeochemistry of dissolved organic carbon and its interactions with climate change. Environ. Sci. Pollut. Res. Int. 16, 714–726.
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6. FACTORS AFFECTING THE BIOAVAILABILITY OF CHEMICALS
Rudel, H., 2003. Case study: Bioavailability of tin and tin compounds. Ecotoxicol. Environ. Saf. 56, 180–189. Schrap, S.M., 1991. Bioavailability of organic chemicals in the aquatic environment. Comp. Biochem. Physiol. C 100, 13–16. Sharma, V.K., 2009. Aggregation and toxicity of titanium dioxide nanoparticles in aquatic environment: A review. J. Environ. Sci. Health A 44, 1485–1495. Tessier, A., Turner, D.R., 1995. Metal Speciation and Bioavailability in Aquatic Systems. Wiley, Hoboken, NJ. Worms, I., Simon, D.F., Hassler, C.S., Wilkinson, K.J., 2006. Bioavailability of trace metals to aquatic microorganisms: Importance of chemical, biological and physical processes on biouptake. Biochimie 88, 1721–1731.
6
Factors Affecting the Bioavailability of Chemicals O U T L I N E 6.1 Introduction
66
6.3 Environmental Bioavailability
68
6.2 Pharmacological Bioavailability
66
Relevant Literature and Cited References 71
Abstract
Bioavailability, uptake, metabolism, storage, and excretion of chemicals constitute toxicokinetics. Bioavailability is the potential for uptake of a substance by a living organism. It is usually expressed as the fraction that can be taken up by the organism in relation to the total amount of the substance available. In pharmacology, the bioavailability is the ratio of the amount of a compound in circulation after its extravenous application and its intravenous injection. In aquatic toxicology, environmental bioavailability is usually relevant. Factors affecting the bioavailability of a chemical depend on the route of uptake, and whether the chemical is in the bottom sediment, dissolved in water, or is a constituent of the organisms. In the case of water-soluble substances, the primary source of toxicant is water, and the bioavailability depends on complex formation, especially with humic substances. Even when water-soluble substances are sediment bound, they reside mainly in pore water. Lipid-soluble substances are taken up especially from sediment or from other organisms. The bioavailability from water decreases with increasing lipophilicity and with increasing amount of dissolved organic carbon or colloids in the aquatic phase. With regard to sediment, both the sediment properties (e.g. grain size) and the amount of organic material in the sediment affect bioavailability. The main abiotic factors affecting bioavailability are oxygenation and pH. As an example, metal speciation, affecting bioavailability, depends very much on the pH. Keywords: toxicokinetics; pharmacological bioavailability; absorbed dose fraction; humus; humic acids; fulvic acids; sediment; metal speciation; total organic carbon; dissolved organic carbon; sorption; nanomaterial bioavailability.
An Introduction to Aquatic Toxicology http://dx.doi.org/10.1016/B978-0-12-411574-3.00006-2
65
© 2014 Elsevier Inc. All rights reserved.
66
6. FACTORS AFFECTING THE BIOAVAILABILITY OF CHEMICALS
6.1 INTRODUCTION The bioavailability of a toxicant, its uptake, metabolism (including transformation), storage, and excretion make up toxicokinetics. Toxicokinetics can thus be defined as the characteristics that affect the amounts of chemicals in the organism (Figure 6.1), and these constitute the material for this and the following chapters (Chapters 7, 8, 9, and 10). The first step of toxicokinetics is bioavailability. Bioavailability is the potential for uptake of a substance by a living organism. It is usually expressed as the fraction that can be taken up by an organism in relation to the total amount of the substance available. Notably, it is always the bioavailable fraction of a compound that participates in the uptake and consecutive responses to a chemical, not the total amount. Consequently, a smaller toxicant load in the environment can cause a larger response, if the environment is associated with increased bioavailability (Figure 6.2). Different aspects of bioavailability in the environmental context are given in Figure 6.3. The bioavailability can be divided into pharmacological bioavailability (how the route of administration affects the potential for uptake of a chemical) and environmental bioavailability (how interactions with the environment affect the potential for uptake of a chemical).
6.2 PHARMACOLOGICAL BIOAVAILABILITY In pharmacology, the bioavailability of a compound is mainly determined by the route of administration. The bioavailability of a compound is virtually complete when the route of
FIGURE 6.1 Representation of different components of toxicokinetics as seen in the toxicant level in an organism as a function of time. (A) An organism is exposed to a chemical. Only a portion of the chemical load is bioavailable (total concentration yellow + green, bioavailable fraction green). (B) The chemical is taken up by the organism. The initial uptake rate is a linear function of the bioavailable fraction of the chemical in the environment. However, after a time, the rate of uptake becomes curvilinear, as the chemical that is taken up is metabolized and excreted. (C) After a given (chemical-specific) time, a steady state is reached upon continuous exposure, where the uptake and metabolism/excretion are equal. (D) If exposure to the toxicant ends, its concentration in the organism decreases. The time course of depuration depends on the excretion mechanisms.
6.2 Pharmacological Bioavailability
67
FIGURE 6.2 A hypothetical example showing that although the total concentration of a chemical is higher in environment A than in environment B, the bioavailable fraction in the latter (red line) can be greater than that in the former (green line).
FIGURE 6.3 Bioavailability of chemicals by location in the environment. A chemical can be available for uptake by an organism if it is (A) contained in the sediment—this is the case especially for organic compounds and benthic organisms or organisms with roots in sediment; (B) in water—this is the case for water-soluble compounds such as most metal cations and small anions. Apparently water-bound organic compounds are often associated with dissolved organic matter or colloidal material in the water column. (C) Chemicals can also be available for uptake from food organisms—normally lipid-soluble compounds are bioavailable through ingestion of food such as prey organisms.
administration is intravenous injection, and varies with intraperitoneal injection, administration in food, administration in the respiratory medium, or penetration through the organismal surface. The bioavailability is given in those cases from the ratio of the systemic exposure from extravascular (e.v.) exposure to that following intravenous (i.v.) exposure, as described by the equation:
F = Aev Div /Biv Dev (6.1)
where F (absorbed dose fraction) is a measure of the bioavailability; A and B are the areas under the (plasma) concentration–time curve following e.v. and i.v. administration, respectively; and Dev and Div are the administered e.v. and i.v. doses. This pharmacological definition of bioavailability is important in aquatic toxicology, as in experimental manipulations
68
6. FACTORS AFFECTING THE BIOAVAILABILITY OF CHEMICALS
FIGURE 6.4 Different routes of administration of a chemical leading to differences in toxicity. A hypothetical example of the response to a toxicant given via (1) intravenous injection, (2) intraperitoneal injection, (3) force feeding (gavage), or (4) exposure to the chemical in the natural environment. Although the molar amount of the chemical that the organism is exposed to can be the same, the amount reaching the target structure may be very different because of the factors affecting (pharmacological) bioavailability.
different toxicants can be administered via intravenous/intraperitoneal injections, via gavage (force feeding), or as a part of the normal diet, or the organisms may be exposed to toxicants via water. It should be remembered that whenever intravenous/intraperitoneal/subcutaneous injections are used, the normal uptake of chemicals from the environment (see Chapter 7) is bypassed. Thus, any such studies can give information about the toxic actions of the compound when in the animal, but the findings cannot be considered environmentally relevant as the possibilities and mechanisms of uptake have not been considered (see Figure 6.4 for a schematic representation of differences in toxicity due to different ways of administering the chemical). Factors that affect the appearance of a compound (drug) in the systemic circulation affect its pharmacological bioavailability. Such factors include interactions with other drugs or food components taken concurrently (altering absorption), first-pass metabolism, intestinal motility, chemical degradation of the drug by intestinal microflora, physical properties of the drug (hydrophobicity, pKa, solubility) and its formulation (including the speed and duration of the release of the active ingredient from the encapsulation), whether the formulation is administered to a fed or fasted organism, rate of gastric emptying, circadian differences, age, and gender.
6.3 ENVIRONMENTAL BIOAVAILABILITY There are three major environmental components from which chemicals may enter organisms in the aquatic environment: water, bottom sediment, and other organisms. The importance of these as uptake sources varies depending on the water solubility of the compound. Highly water soluble compounds are preferentially taken up from the aqueous phase. Even if the compounds are largely found in sediment, their location and uptake site will be in the pore water. Lipophilic compounds will be obtained either from sediment or, especially, from food (i.e. other organisms). The deposition history of a compound will also affect its availability. If most of the compound has accumulated to bottom sediments over time, the potential for
6.3 Environmental Bioavailability
69
uptake from these sediments will be highest. Finally, different organisms can have markedly different loads of contaminants depending on their feeding habits, their movements between differently contaminated areas, etc. As an example, a sediment-bound contaminant can be transferred in the food web quite differently in the presence of rooted green plants than in the presence of pelagic unicellular algae. Regardless of the main uptake route of the chemical, the factors affecting bioavailability are essentially the same. They are, first, the complex formation of the toxicant with naturally occurring compounds; second, their lipophilicity; and, third, their resemblance to compounds that are specifically taken up. Naturally, the stability of the compound, which may be different in different compartments of aquatic systems, will also influence how it can be taken up. Strictly speaking, this is not an aspect of bioavailability, but a part of the environmental fate of the toxicant. However, the interactions of the chemical with the environment are an important determinant of the subsequent uptake, and therefore must be mentioned at this point. In the bioavailability of compounds one needs to consider both the water and the sediment properties, and also how other organisms affect the properties of compounds taken up. An important component of such organismic interactions is that microorganisms, in particular, may take up substances and render them inaccessible to other organisms that do not eat the microorganisms. Also, when considering bioavailability, the delivery of compounds from the atmosphere by rainfall (frequency is more important than amount) must be taken into account. The total organic carbon content (TOC) and dissolved organic carbon content (DOC) have intimate association with bioavailability. Largely, this is due to many contaminants forming complexes with the carbon compounds. In aquatic systems the most important complex-forming compounds are humic substances. Humic substances are usually large colloidal molecules with several carboxylic acid and phenolic groups. They are usually divided into two classes: the larger humic acids (molecular weight (MW) > 1000, up to 100,000) and the smaller fulvic acids (MW usually < 1000). Because the humic substances contain carboxylate groups, they are normally acidic with an overall negative charge. In solution they usually behave as biphasic weak acids with a pK value around 4. The humic substances are formed by the breakdown of plant matter, and their exact structure is sitedependent, depending on the plants in the environment. Humic substances can also form a major part of the nutrition of prokaryotes. As the humic substances have an overall negative charge, they can form complexes with positively charged metal ions (and other positively charged compounds). Complex formation is especially pronounced with divalent cations, such as Fe2+, Mg2+, and Ca2+. The bioavailability of metals has been studied very intensively. In addition to complex formation, especially with humus, this is affected by the type of metal compound. For example, sulfide minerals may be encapsulated in quartz or other chemically inert minerals, and despite high total concentrations of metals in sediment containing these minerals they may not be bioavailable and thus their environmental effects may remain small. Consequently, as an example, the type of ore containing the metal affects the toxicity of mining effluents to aquatic systems. If the aquatic environment has reducing conditions, for example if they are hypoxic, metal ions are associated with sulfides, e.g. insoluble FeS is formed. Most metal sulfides are poorly soluble, and consequently quite immobile as long as they remain in a chemically reducing environment. Because of this, their bioavailability is reasonably low. Consequently, oxygenation of the aqueous medium (and the sediment) will affect the bioavailability of
70
6. FACTORS AFFECTING THE BIOAVAILABILITY OF CHEMICALS
metals. The reason why arsenic has become a major pollutant is that it is released from the sulfide-based iron ores when they come into contact with oxygen-containing water. In addition to affecting the fate of metals, oxygenation affects both the properties and stability of organic contaminants. The apparent presence and bioavailability of organic toxicants is different in oxic and anoxic sediments. Another sediment property affecting the bioavailability of organic contaminants is the amount of other organic material in the sediment. Increasing organic material tends to increase the sorption of an organic chemical to the sediment, reducing its availability in the aquatic phase. In general, aquatic bioavailability has close interactions with how compounds are moving between bottom sediments and water, and the final equilibria between the two compartments. Particle size and resulting total surface area available for adsorption are both important factors in adsorption processes in the sediments, and can affect the bioavailability of compounds. Small particles with large surface-area-to-mass ratios allow more adsorption than an equivalent mass of large particles with small surface-area-to-mass ratios. This is most important with regard to nanomaterials. Because of the surface-area-to-mass dependence of bioavailability, the toxicity of nanomaterials can be strongly affected by the size of particles in the formulations. Since the sedimentation of nanomaterials is affected by the way a test is executed, markedly different bioavailabilities and toxicities of nanomaterials have been reported. Reduced adsorption of compounds to sediments can also affect their bioavailability by affecting the dissolved concentration of a compound in the water surrounding the sediment. In the aqueous phase, the bioavailability of organic contaminants depends on their partitioning between the organic phase and water. Lipophilicity is also an important aspect of chemical uptake in organisms, and its determination and main discussion are given in Chapter 7. However, it needs to be pointed out here that, because of the interactions between organic contaminants and other organic materials in water, the bioavailability of organic contaminants from water will decrease with increasing dissolved organic carbon content and increasing amount of colloids in the aquatic phase. Apart from oxygenation, another abiotic factor affecting bioavailability is pH. The effects of pH have been studied especially with regard to the speciation (and solubility) of metals, as exemplified for aluminum in (Figure 6.5). At pH values above neutral, aluminum ions form insoluble compounds; between pH values 5 and 7, the metal exists FIGURE 6.5 Approximate proportions of the different aluminum species (free cations, hydroxides) as a function of pH.
6.3 Environmental Bioavailability
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largely as soluble hydroxides; and at pH values below 5, it exists largely as toxic free Al3+ ions. Because of the pH effects, the bioavailability of metals and other compounds may be markedly different in bulk water and in the vicinity of (fish) gills, since there is a large pH gradient in the water from the gills to the bulk water. Also, the mode of toxicity of metals and other compounds may be different at different pH values. Again, as an example, aluminum appears to be mainly a respiratory toxicant at intermediary pH values (5–7), largely because it precipitates on gill filaments, increasing the diffusion distance of oxygen. At lower pH values, it appears to be an ionoregulatory toxicant. The hardness of water (essentially its salinity) also affects bioavailability, mostly of ionic compounds. The effect is largely due to a change in the probability of a toxic ion being taken up instead of a nontoxic one in the uptake site. The bioavailability of metals is often calculated using the biotic ligand model (BLM), which seeks to take into account the effects of complex formation, abiotic environmental factors such as pH, and metal interactions (for details, see Chapter 18). Many of these factors vary seasonally and temporally, and most factors are interrelated. Consequently, changing one factor may affect several others. In addition, generally poorly understood biological factors seem to influence bioaccumulation of metals and thereby affect any predictions of their toxicity: an important factor here is the type of aquatic environment. Uptake of ions occurs very differently in marine and freshwater environments. Consequently, what is a useful model in freshwater may not be accurate in the marine environment. The modeling of toxicant accumulation in organisms is discussed further in Chapter 18.
Relevant Literature and Cited References Andrady, A.L., 2011. Microplastics in the marine environment. Mar. Pollut. Bull. 62, 1596–1605. Beckett, R., Jue, Z., Giddings, J.C., 1987. Determination of molecular weight distributions of fulvic and humic acids using flow field–flow fractionation. Environ. Sci. Technol. 21, 289–295. Boudou, A., Ribeyre, F., 1997. Aquatic ecotoxicology: From the ecosystem to the cellular and molecular levels. Environ. Health Perspect. 105 (Suppl. 1), 21–35. Burton Jr., G.A., 2010. Metal bioavailability and toxicity in sediment. Crit. Rev. Environ. Sci. Technol. 40, 852–907. Camargo, J.A., 2003. Fluoride toxicity to aquatic organisms: A review. Chemosphere 50, 251–264. Chapman, P.M., Wang, F., Janssen, C., Persoone, G., Allen, H.E., 1998. Ecotoxicology of metals in aquatic sediments: Binding and release, bioavailability, risk assessment, and remediation. Can. J. Fish Aquat. Sci. 55, 2221–2243. Farrington, J.W., 1991. Biogeochemical processes governing exposure and uptake of organic pollutant compounds in aquatic organisms. Environ. Health Perspect. 90, 75–84. Haitzer, M., Hoss, S., Traunspurger, W., Steinberg, C., 1998. Effects of dissolved organic matter (DOM) on the bioconcentration of organic chemicals in aquatic organisms: A review. Chemosphere 37, 1335–1362. Hamelink, J.L., Landrum, P.F., Bergman, H.L., Benson, W.H., 1994. Bioavailability: Physical, Chemical and Biological Interactions. CRC Press, Boca Raton, FL. Haws, N.W., Ball, W.P., Bouwer, E.J., 2006. Modeling and interpreting bioavailability of organic contaminant mixtures in subsurface environments. J. Contam. Hydrol. 82, 255–292. Henry, T.B., Petersen, E.J., Compton, R.N., 2011. Aqueous fullerene aggregates (nC60) generate minimal reactive oxygen species and are of low toxicity in fish: A revision of previous reports. Curr. Opin. Biotechnol. 22, 533–537. Markich, S.J., 2002. Uranium speciation and bioavailability in aquatic systems: An overview. Sci. World J. 2, 707–729. Navarro, E., Baun, A., Behra, R., Hartmann, N.B., Filser, J., Miao, A.J., Quigg, A., Santschi, P.H., Sigg, L., 2008. Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17, 372–386. Porcal, P., Koprivnjak, J.F., Molot, L.A., Dillon, P.J., 2009. Humic substances—part 7: The biogeochemistry of dissolved organic carbon and its interactions with climate change. Environ. Sci. Pollut. Res. Int. 16, 714–726.
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6. FACTORS AFFECTING THE BIOAVAILABILITY OF CHEMICALS
Rudel, H., 2003. Case study: Bioavailability of tin and tin compounds. Ecotoxicol. Environ. Saf. 56, 180–189. Schrap, S.M., 1991. Bioavailability of organic chemicals in the aquatic environment. Comp. Biochem. Physiol. C 100, 13–16. Sharma, V.K., 2009. Aggregation and toxicity of titanium dioxide nanoparticles in aquatic environment: A review. J. Environ. Sci. Health A 44, 1485–1495. Tessier, A., Turner, D.R., 1995. Metal Speciation and Bioavailability in Aquatic Systems. Wiley, Hoboken, NJ. Worms, I., Simon, D.F., Hassler, C.S., Wilkinson, K.J., 2006. Bioavailability of trace metals to aquatic microorganisms: Importance of chemical, biological and physical processes on biouptake. Biochimie 88, 1721–1731.