PRINCIPLES OF ENVIRONMENTAL TOXICOLOGY AND CONTAMINATION (PART II)

Table of Contents

1. Index
2. UNIT 5 - Transport and fate of contaminants in the environment
   1. Introduction
   2. Transport processes
   3. Environmental persistence and transformation processes
   4. Bioaccumulation
   5. Environmental fate models
   6. Brief conclusion
3. UNIT 6 - Principles of toxicokinetics and toxicodynamics
4. UNIT 7 - Biotransformation
5. UNIT 8 - Toxicity Testing
6. Glossary of key terms associated with environmental toxicology

Bioaccumulation

Environmental persistence alone does not render a chemical problematic in the environment. If the chemical cannot enter the body of organisms, then it would pose no threat of toxicity. Once absorbed, the chemical must accumulate in the body to sufficient levels to cause toxicity. Bioaccumulation is defined as the process by which organisms accumulate chemicals both directly from the abiotic environment (i.e., air, water, soil) and from dietary sources (trophic transfer). Therefore, this process consists in the sorption of contaminants in the organisms faster than its elimination. Many organic environmental chemicals are largely taken up by organisms by passive diffusion. On the other hand, metals cannot simply diffuse across plasma membranes, being generally transported by ion pumps or channels that otherwise would transport essential ions like sodium or calcium. Primary sites of uptake include membranes of the lungs, gills, and gastrointestinal tract (GIT). Despite the integument (skin) and associated structures (scales, fur, feathers, etc.) provide a protective barrier against many environmental insults, significant dermal uptake of some chemicals can happen. Chemicals that demonstrate tendency to bioaccumulate are usually organic, non-ionised and very poorly soluble or insoluble in water. In this way, the organic chemicals must traverse the lipid bilayer of membranes to enter the body, and thus, the bioaccumulation potential of chemicals is positively correlated with lipid solubility (lipophilicity).

The aquatic environment is the major site at which lipophilic chemicals traverse the barrier between the abiotic environment and the biota. This happens because rivers, lakes, and oceans serve as sinks for these chemicals; and by the fact that aquatic organisms pass large quantities of water across their respiratory membranes (i.e., gills), allowing for the efficient extraction of the chemicals from the water. For example, fish can accumulate tremendous amounts of contaminants directly from the medium due to the large area of gill filaments, their intimate contact with the water and also the high flow rate of water over them. Given these characteristics a contaminant with a high partition coefficient between lipid membranes and water, is easily uptaked.

Aquatic organisms can bioaccumulate lipophilic chemicals and reach body concentrations that are several orders of magnitude greater than the chemical concentration found in the environment (Table 2). The degree to which aquatic organisms accumulate xenobiotics from the environment is widely dependent upon the lipid content of the organism because the body lipids serve as the primary site of chemicals retention (Figure 3).

Table 2 - Bioaccumulation of some environmental contaminants by fish.

Source: LeBlanc GA. (1994) and Hodgson E. (2010).

^aBioaccumulation factor is defined as the ratio of the chemical concentration in the fish and in the water at steady-state equilibrium.

Figure 3 - Relationship between lipid content of a variety of organisms sampled from Lake Ontario and whole-body PCB concentration. 
Source: Oliver & Niimi (1988) and Hodgson E. (2010).

Most aquatic animals directly exchange ions with the surrounding water to maintain water-salt balance. However, many metals have affinities for ion transport systems (usually located on gills or other body surfaces), as referred above, and thus direct uptake of metals from water can be an important exposure route.

Both organic chemicals and metals can also be transferred along food chains from prey organism to predator (trophic transfer). For highly lipophilic chemicals, this transfer can result in increasing concentrations of the chemical with each progressive link in the food chain. In other words, the higher trophic level organisms are exposed to enriched concentrations of contaminants in their tissues via their prey. This process is known as biomagnification. There are now many well-known cases of chemicals biomagnifying in food webs to the point that toxic effects are exhibited in organisms that may have had no direct exposure to the chemical itself at its point of application. The polychlorinated biphenols (PCBs), organochlorine insecticides, and organometallic compounds (methyl mercury and organic selenium species) are a few examples. DDT is also a well-known example of bioaccumulation and resultant biomagnification. The transfer of DDT in the food chain was responsible for the decline of many bird-eating raptor populations, which contributed to the decision to ban the use of this pesticide in the United States (as mentioned in unit 4). However, researchers have shown that some contaminants such as PAHs, do biomagnify less with increasing trophic level. Notwithstanding, these contaminants are found in marine organisms at high trophic levels.

Bioaccumulation factor (BAF) or Bioconcentration factor (BCF) - describe the tendency of a chemical to be more concentrated in an organism than in its environment. The BAF or BCF is calculated by dividing the concentration of the chemical in the organism by the concentration of the chemical in the water, soil, or sediment, in which it lives. BAFs assume that exposure has occurred through all potential routes, including ingestion of contaminated foods and direct uptake from the environmental medium. BCFs refer to water exposures and are applied typically only to aquatic organisms. However, BCFs have been used considering pore-water transfer of chemicals to invertebrates in mesic soil environments. Bioaccumulation and bioconcentration assume that the organism is at a steady state with the chemical in its environment and assumes net uptake and so does not account for the ability or rate at which an organism metabolizes the chemical. Additionally, the BCFs or BAFs are often species and site specific, and a lack of consideration of species-specific toxicokinetics may yield misleading conclusions.

An example of bioaccumulation and resultant biomagnification along a generic food chain can be seen in figure 4. A chemical that bioaccumulates by a factor of 2, regardless of whether the contaminant source is food or water, would have the potential to magnify at each trophic level. This leads to high levels in the birds of prey relative to that observed in the abiotic environment (fig. 4).

Figure 4 - Bioaccumulation of a chemical along a generic food chain. In this simplistic paradigm, the amount of the chemical in the water is assigned an arbitrary concentration of 1, and it is assumed that the chemical will bioaccumulate either from the water to the fish or from one trophic level to another by a factor of 2. Circled numbers represent the concentration of chemical in the respective compartment. Numbers associated with arrows represent the concentration of chemical transferred from one compartment to another. Source: Hodgson E. (2010).

For many compounds, bioaccumulation is typically much greater from water than from food, and it is unlikely that an organism would accumulate a chemical to the same degree from both sources. However, bioaccumulation is thought to be primarily derived from the diet for some elements such as selenium.

In addition, for many trace metals, there appears to be a major difference between fish and invertebrates in the bioaccumulation patterns. Fish tend to have poor assimilation efficiencies for many metals. On the other hand, invertebrates tend to have very high assimilation efficiencies for metals from their diets. Thus, it is extremely important to understand the dietary route of exposure in invertebrates. This difference has practical implications in the setting of water quality criteria, because the susceptibility of invertebrates to metals is likely underestimated from toxicity tests that use only dissolved exposures.

To conclude, the exposure routes and the physical and biochemical make-up of the animal are factors that affect the transfer of chemicals in the aquatic environment.

Note: Bioaccumulation of lipophilic compounds can lead to a delay in the onset of toxicity because the contaminant may be initially sequestered in lipid deposits. However, the contaminant is mobilized to target sites of toxicity when these lipid stores are utilized. For example, lipid stores are frequently mobilized in preparation for reproduction. The lipid loss can result in the release of lipophilic contaminants rendering them available for toxic action. As a consequence, the mortality of adult organisms can occur as they approach reproductive maturity. Lipophilic chemicals also can be transferred to the offspring in lipids associated with the milk of mammals or with the yolk of oviparous organisms. This can result in toxicity to the offspring that was not evident in the parental organisms.

To better understand the bioaccumulation process, see the following video:

https://www.youtube.com/watch?v=fdTV3F9k1IA

4.1 FACTORS THAT INFLUENCE BIOACCUMULATION

The propensity for an environmental contaminant to bioaccumulate is influenced by several factors:

• Lipophilicity is a main determinant of the bioaccumulation potential of a chemical, as referred above. Nevertheless, lipophilic chemicals also have greater propensity to sorb to sediments thus rendering them less available to bioaccumulate. For example, fish from eutrophic lakes*, having high suspended solid levels, have been shown to accumulate less DDT than fish from oligotrophic lakes* that have low suspended solid contents. In addition, the sorption of benzo[a]pyrene to humic acids reduced its propensity to bioaccumulate in sunfish by a factor of 3.
• Environmental persistence. The degree to which a chemical bioaccumulates is dependent on their concentration present in the environment. Contaminants that are readily eliminated from the environment will usually not be available to bioaccumulate. An exception would be cases where the contaminant is continuously introduced into the environment (e.g.: receiving water of an effluent discharge).
• Fate, transformation and elimination of the contaminant. Once absorbed by the organism, the fate of the contaminant will influence its bioaccumulation. Chemicals that are readily biotransformed (see Chapter 7) are rendered less lipid soluble and more water soluble. Therefore, the biotransformed chemical is less likely to be sequestered in the lipid compartments and, consequently, is more likely to be eliminated from the body. As can be seen in table 3, chemicals that are susceptible to biotransformation, bioaccumulate much less than would be predicted based upon lipophilicity. Additionally, differences in chemical elimination rates contribute to species differences in bioaccumulation.

Table 3 - Predicted and measured bioaccumulation factors in fish of chemicals that differ in susceptibility to biotransformation.

Predicted bioaccumulation factors were based upon their relative lipophilicity as described by D. Mackay (1982). Source: Hodgson E. (2010).

More information about oil bioaccumulation in aquatic environment can be found in the following articles:

http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0074476