## 4.1.6. Food chain transfer

Auteur: Nico van den Brink

Reviewers: Kees van Gestel. Jan Hendriks

Learning objectives:

You should be able to:

- Mention the chemical properties determining the potential of chemicals to accumulate in food chains
- Explain the role of biological and ecological factors in the food-chain accumulation of chemicals

Keywords: biomagnification, food-chain transfer,

Accumulation of chemicals across different trophic levels.

Chemicals may be transferred from one organism to another. Grazers will ingest chemicals that are in the vegetation they eat. Similarly, predators are exposed to chemicals in their prey items. This so-called food web accumulation is governed by properties of the chemical, but also by some traits of the receiving organism (e.g. grazer or predator).

Chemical properties driving food web accumulation

Some chemicals are known to accumulate in food webs, reaching the highest concentrations in top-predators. Examples of such chemicals are organochlorine pesticides like DDT and brominated flame retardants (e.g. PBDEs; see section on POPs). Such accumulating chemicals have a few properties in common: they need to be persistent and they need to have affinity for the organismal body. Organic chemicals with a relatively high log Kow, indicating a high affinity for lipids, will enter organisms quite effectively (see section on Bioconcentration and kinetics modelling). Once in the body, these chemicals will be distributed to lipid rich tissues, and excretion is rather limited. In case of persistent chemicals that are not metabolised, concentrations will increase over time when uptake is higher than excretion. Furthermore, such chemicals are likely to be passed on to organisms at the next trophic level in case of prey-predator interactions. Some of these chemicals may be metabolised by the organism, most often into more water soluble metabolites (see section on Xenobiotic metabolism & defence). These metabolites are more easily excreted, and in this way concentrations of metabolizable chemicals do not increase so much over time, and will therefore also transfer less to higher trophic levels. The effects of metabolism on the internal concentrations of organisms is clearly illustrated by a study on the uptake of organic chemicals by different aquatic species (Kwok et al., 2013). In that study the uptake of persistent chemicals (organochlorine pesticides; OCPs) was compared with the uptake of chemicals that may be metabolised (polycyclic aromatic hydrocarbons; PAHs). The authors compared shrimps with fish, the former having a limited capacity to metabolise PAHs while fish can. Figure 1 shows the Biota-to-Sediment Accumulation Factors (BSAFs; see section on Bioaccumulation), which is the ratio between the concentration in the organism and in the sediment. It is shown that OCPs accumulate to a high extent in both species, reflecting persistent, non-metabolizable chemicals. For PAHs the results are different per species, fish are able to metabolise and as a result the concentrations of PAHs in the fish are low, while in shrimp, with a limited metabolic capacity, the accumulation of PAHs is comparable to the OCPs. These results show that not only the properties of the chemicals are of importance, but also some traits of the organisms involved, in this case the metabolic capacity.

Figure 1. Biota–sediment accumulation factors organochlorine pesticides (OCPs) and polycyclic aromatic hydrocarbons (PAHs) in fish and shrimp. Redrawn from Kwok et al. (2013).

Effects of species traits and food web structure on food web accumulation

Food-web accumulation of chemicals is driven by food uptake. At lower trophic levels, most organisms will acquire relatively low concentrations from the ambient environment. First consumers, foraging on these organisms will accumulate the chemicals of all of them, and in case of persistent chemicals that enter the body easily, concentrations in the consumers will be higher than in their diet. Similarly, concentrations will increase when the chemicals are transferred to the next trophic level. This process is called biomagnification, indicating increasing concentrations of persistent and accumulative chemicals in food webs. The most iconic example of this is on the increasing concentrations of DDTs in fish eating American Osprey (Figure 2), a casus which has led to the ban of a lot of organochlorine chemicals.

Figure 2. Example of biomagnification of DDT in an aquatic food web of ospreys. Slightly modified from: http://naturalresources.anthro-seminars.net/concepts/ecological-concepts-biomagnification/.

Since biomagnification along trophic levels is food driven, it is of importance to include diet composition into the studies. This can be explained by an example on small mammals in the Netherlands. Two similar small mammal species, the bank vole (Myodes glareolus) and the common vole (Microtus arvalis) co-occur in larger part of the Netherlands. Although the species look very similar, they are different in their diet and habitat use. The bank vole is a omnivorous species, inhabiting different types of habitat while the common vole is strictly vegetarian living in pastures. In a study on the species-specific uptake of cadmium, diet items of both species were analysed, indicating nearly 3 orders of magnitudes differences in cadmium concentrations between earthworms and berries from vegetation (Fig 3A, van den Brink et al., 2010). Stable isotopic ratios of carbon and nitrogen were used to assess the general diets of the organisms. The common vole ate mostly stinging nettle and grass, including seeds, while the bank vole showed to forage on grass herbs and earthworms. This difference in diet was reflected in increased concentrations of cadmium in the bank vole in comparison to the common vole (both inhabiting the same area). The concentrations of one bank vole appeared to be extremely low (red diamond in Figure 3b), and initially this was considered to be an artefact. However, detailed analysis of the stable isotopic ratios in this individual revealed that it had foraged on stinging nettle and grass, hence a diet more reflecting the common vole. This emphasises once more that organisms accumulate through their diet (you accumulate what you eat!)

Figure 3. Left: Concentrations of cadmium in diet items of small mammals collected in the Plateaux area near Eindhoven, the Netherlands; Right: Cadmium concentrations in kidneys of bank voles and common voles collected in the Plateaux area. See text for further explanation. Redrawn from van den Brink et al. (2010).

Case studies

Orcas or Killer whales (Orcinus orca) are large marine predatory mammals, which roam all around the oceans, from the Arctic to the deep south region of the Antarctic. Although they appear ubiquitous around the world, generally different pods of Orcas occur in different regions of the marine ecosystem. Often, each pod has developed specialised foraging behaviours targeted at specific prey species. Although Orcas are generally apex top-predators at the top of the (local) food web, the different foraging strategies would suggest that exposure to accumulating chemicals may differ considerably between pods. This was indeed shown to be the case in a very elaborate study on different pods of Orcas of the West-coast of Canada by Ross et al. (2000). In the Vancouver region there is a resident pod while the region is also often visited by two transient groups of Orcas. PCB concentrations were high in all animals, but the transient animals contained significantly higher levels. The transient whales mainly fed on marine mammals, while the resident animals mainly fed on fish, and this difference in diet was thought to be the cause of the differences in PCB levels between the groups. In that study, it was also shown that PCB levels increased with age, due to the persistence of the PCBs, while female orcas contained significant lower concentrations of PCBs. The latter is caused by the lactation of the female Orcas during which they feed their calves with lipid rich milk, containing relatively high levels of (lipophilic) PCBs. By this process, females offload large parts of their PCB body burden, however by transferring these PCBs to their developing calves (see also Figure 3 in the section on Bioaccumulation). A recent study showed that although PCBs have been banned for decades now, they still pose threats to populations of Orcas (Deforges et al., 2018). In that study, regional differences in PCB burdens were confirmed, likely due to differences in diet preferences although not specifically mentioned. It was shown that PCB levels in most of the Orca populations were still above toxic threshold levels and concerns were raised regarding the viability of these populations. This study confirms that 1) Orcas are exposed to different levels of PCBs according to their diet, which influences the biomagnification of the PCBs, 2) Orca populations are very inefficient in clearing PCBs from the individual due to little metabolism but also from the population due to the efficient maternal transfer from mother to calve, and 3) persistent, accumulating chemicals may pose threats to organisms even decades after their use. Understanding the mechanisms and processes underlying the biomagnification of persistent and toxic compounds is essential for a in depth risk assessment.

References

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