4.1.1. Bioaccumulation

Author: Joop Hermens

Reviewers: Kees van Gestel and Philipp Mayer

Learning objectives:

You should be able to

define and explain different bioaccumulation parameters.
Mention different biological factors that may affect bioaccumulation.

Key words: Bioaccumulation, lipid content

Introduction: terminology for bioaccumulation

The term bioaccumulation describes the transfer and accumulation of a chemical from the environment into an organism.” For a chemical like hexachlorobenzene, the concentration in fish is more than 10,000 times higher than in water, which is a clear illustration of “bioaccumulation”. A chemical like hexachlorobenzene is hydrophobic, so has a very low aqueous solubility. It therefore prefers to escape the aqueous phase to enter (or partition into) a more lipophilic phase such as the lipid phase in biota.

Uptake may take place from different sources. Fish mostly take up chemicals from the aqueous phase, organisms living at the sediment-water interphase are exposed via the overlying water and sediment particles, organisms living in soil or sediment via pore water and by ingesting soil or sediment, while predators will be exposed via their food. In many cases, uptake is related to more than one source. The different uptake routes are also reflected in the parameters and terminology used in bioaccumulation studies. The different parameters include the bioconcentration factor (BCF), bioaccumulation factor (BAF), biomagnification factor (BMF) and biota-to-sediment or biota-to-soil accumulation factor (BSAF). Figure 1 summarizes the definition of these parameters. Bioconcentration refers to uptake from the aqueous phase, bioaccumulation to uptake via both the aqueous phase and the ingestion of sediment or soil particles, while biomagnification expresses the accumulation of contaminants from food.

Figure 1. Parameters used to describe the bioaccumulation of chemicals.

C_aq concentration in water (aqueous phase)

C_org concentration in organism

C_f concentration in food

C_s concentration in sediment or soil

Please note that the bioaccumulation factor (BAF) is defined in a similar way as the bioconcentration Factor (BCF), but that uptake can be both from the aqueous phase and the sediment or soil and that the exposure concentration usually is expressed per kg dry sediment or soil. Other definitions of the BAF are possible, but we have followed the one from Mackay et al. (2013). “The bioaccumulation factor (BAF) is defined here in a similar fashion as the BCF; in other words, BAF is CF/CW at steady state, except that in this case the fish is exposed to both water and food; thus, an additional input of chemical from dietary assimilation takes place”.

All bioaccumulation factors are steady state constants: the concentration in the organism constant and the organisms is in equilibrium with its surrounding phase. It will take time before such an steady state is reached. Steady state is reached when uptake rate (for example from an aqueous phase) equals the elimination rate. Models that include the factor time in describing the uptake are called kinetic models; see section on Bioaccumulation kinetics.

Effect of biological properties on accumulation

Uptake of chemicals is determined by properties of both the organism and the chemical. For xenobiotic lipophilic chemicals in water, organism-specific factors usually play a minor role and concentrations in organisms can pretty well be predicted from chemical properties (see section on Structure-property relationships). For metals, on the contrary, uptake is to a large extent determined by properties of the organism, and a direct consequence of its mineral requirements. A chemical with low bioavailability (low uptake compared to concentration in exposure medium) may nevertheless accumulate to high levels when the organism is not capable of excreting or metabolising the chemical.

Factors related to the organism are:

Fat content. Because lipophilic chemicals mainly accumulate in the fat of organisms, it is reasonable to assume that lipid rich organisms will have higher concentrations of lipophilic chemicals. See Figure 2 for an example of bioconcentration factors of 1,2,4-trichlorobenzene in a number of organisms with varying lipid content. This was one of the explanations for the high PCB levels in eel (high lipid content) in Dutch rivers and seals from the Wadden Sea. Nevertheless, large differences are still found between species when concentrations are expressed on a lipid basis. This may e.g. be explained by the fact that lipids are not all identical: PCBs seem to dissolve better in lipids from anchovies than in lipids from algae (see data in Table 1). Also more recent research has shown that not all lipids are the same and that differences in bioaccumulation between species may be due to differences in lipid composition (Van der Heijden and Jonker, 2011). Related to this is the development of BCF models that are based on multiple compartments and that make a separation between storage and membrane lipids and also include a protein fraction as additional sink (Armitage et al., 2013). In this model, the overall distribution coefficient D_BW (or BCF) is estimated via equation 1. The equation is using distribution coefficients because the model also “accounts for the presence of neutral and charged chemical species” (Armitage et al., 2013).

$BCF\quad or\quad D_{BW} = f_{SL} D_{SL-W} + f_{ML} D_{ML-W} + f_{NLOM} D_{NLOM-W} + f_W$

D_BW	overall organism-water distribution coefficient (or surrogate BCF) at a given pH
D_SL-W	storage lipid-water distribution ratio
D_ML-W	membrane lipid-water distribution ratio
D_NLOM-W	sorption coefficient to NLOM (non-lipid organic matter, for example proteins)
f_SL	fraction of storage lipids
f_ML	fraction of membrane lipids
f_NLOM	fraction of non-lipid organic matter (e.g. proteins, carbohydrates)
f_W	fraction of water

Sex: Chemicals (such as DDT, PCB) accumulated in milk fat may be transferred to juveniles upon lactation. This was found in marine mammals. In this way, females have an additional excretion mechanism. A typical example is shown in Figure 3, taken from a study of Abarnou et al. (1986) on the levels of organochlorinated compounds in the Antarctic dolphin Cephalorhyncus commersonii. In males, concentrations increase with increasing age, but concentrations in mature females decrease with increasing age.
Weight: (body mass) of the organism relative to the surface area across which exchange with the water phase takes place. Smaller organisms have a larger surface-to-volume ratio and the exchange with the surrounding aqueous phase is faster. Therefore, although lipid normalized concentrations will be the same at equilibrium, this equilibrium is reached earlier in smaller than in larger organisms.
Difference in uptake route. The relative importance of uptake through the skin (in fish e.g. the gills) and (oral) uptake through the digestive system. It is generally accepted that for most free-living organism’s direct uptake from the water dominates over uptake after digestion in the digestive tract.
Metabolic activity. Even at the same weight or the same age, the balance between uptake and excretion may change due to an increased metabolic activity, e.g. in times of fast growth or high reproductive activity.

Figure 2. The influence of lipid content on the bioconcentration of 1,2,4-trichlorobenzene in different fish species (reproduced using data from Geyer et al., 1985).

Table 1. Mean PCB concentrations in algae (Dunaliella spec.), rotifers (Brachionus plicatilis) and anchovies larvae (Angraulis mordax), expressed on a dry-weight basis and on a lipid basis. From Moriarty (1983).

Organism	Lipid content (%)	PCB-concentration based on dry weight (µg g^-1)	PCB-concentration based on lipid weight (µg g^-1)	BCF based on concentration in the lipid phase
algae	6.4	0.25	3.91	0.48 x 10⁶
rotifer	15.0	0.42	2.80	0.34 x 10⁶
fish (anchovies) larvae	7.5	2.06	27.46	13.70 x 10⁶

Figure 3. Concentrations of DDT in dolphins of different age and the difference between male and female dolphins Redrawn from Abernou et al. (1986) by Wilma IJzerman.

Cited references

Abarnou, A., Robineau, D., Michel, P. (1986). Organochlorine contamination of commersons dolphin from the Kerguelen islands. Oceanologica Acta 9, 19-29.

Armitage, J.M., Arnot, J.A., Wania, F., Mackay, D. (2013). Development and evaluation of a mechanistic bioconcentration model for ionogenic organic chemicals in fish. Environmental Toxicology and Chemistry 32, 115-128.

Geyer, H., Scheunert, I., Korte, F. (1985). Relationship between the lipid-content of fish and their bioconcentration potential of 1,2,4-trichlorobenzene. Chemosphere 14, 545-555.

Mackay, D., Arnot, J.A., Gobas, F., Powell, D.E. (2013). Mathematical relationships between metrics of chemical bioaccumulation in fish. Environmental Toxicology and Chemistry 32, 1459-1466.

Moriarty, F. (1983). Ecotoxicology: The Study of Pollutants in Ecosystems. Publisher: Academic Press, London.

Van der Heijden, S.A., Jonker, M.T.O. (2011). Intra- and interspecies variation in bioconcentration potential of polychlorinated biphenyls: are all lipids equal? Environmental Science and Technology 45, 10408-10414.