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Effects of contaminants on seabirds: an energetics approach

Periodic Reporting for period 1 - ECOSEA (Effects of contaminants on seabirds: an energetics approach)

Reporting period: 2017-12-04 to 2019-12-03

Metals and industrial substances used to make every-day objects such as computers, mobile phones, frying pans and waterproof clothes, make their way into the natural environment. These substances are considered to be environmental contaminants and can have a devastating impact on wildlife, in particular predators such as seabirds. However, our understanding of how and when seabirds become contaminated and the consequences of this contamination is limited. While we know that seabirds can ingest these contaminants by eating their prey, it is unclear why some species and some individuals within species have higher contaminant levels than others and what the consequences of this might be. Investigating these questions is critical to understand toxic effects and potential wildlife population declines. Mercury (a heavy metal) and perfluorinated compounds are particularly important to study because they have long residence time in the environment, and in animal and human bodies, with known negative impacts on them. Animals have physiological mechanisms to eliminate contaminants form their bodies. However, these mechanisms are not always effective and can be very costly in terms of energy and nutrients. Contaminants can also increase the susceptibility of animals to disease, or/and make disease more dangerous for them. Yet, the interaction between contaminants and disease is poorly known in seabirds, and so are the consequences of it on energy use, reproduction and mortality of seabirds. The aim of the ECOSEA project was to study the levels and effects of natural (metals) and man-made (perfluorinated substances) contaminants in a declining British seabird: the European shag (hereafter “shag”). The study site was the Isle of May, Firth of Forth, Scotland, an environment which has received a plethora of contaminants over 200 years of intense industrial and urban activities. Shags have been monitored here for more than 30 years, so that we know the age, sex and reproductive history of many of them. Specific objectives of ECOSEA were the following: Aim 1) describe what prey the shags feed on, and where precisely they capture them, in order to understand if different prey, as well as other bodily characteristics such as sex, size and age, explain contaminant level differences between birds; Aim 2) understand if contaminants constitute an energetic costs for the shags; Aim 3) determine if there is a relationship between contaminant levels and the number of parasites present in the stomach of the birds (nematode worms, Contracaecum rudolphii); and 4) measure the combined effects of contaminants and parasites on reproduction.
In order to address ECOSEA aims we sampled 44 shags in summer 2018 during reproduction. We collected a small blood sample and feathers, equipped birds with miniaturized recorders that can measure GPS position, diving depth and bird activity, and counted the number of parasites in their stomachs by endoscopy. We used stable isotope analyses of blood to study the birds’ diet. The ratio of the stable isotopes of carbon (13C/12C) indicates the origin of their food (from terrestrial or marine environments, from the water column or the seabed). On the other hand, the ratio of the stable isotopes of nitrogen (15N/14N) represents the position of the animal in the food web (from first-level consumers up to top predators). We also used compound-specific stable nitrogen isotopes of amino acids (molecules that combine to form proteins), which is a novel, powerful technique that complements classic isotopic analyses by giving additional information on diet. We measured 11 metals and 17 perfluorinated compounds in the birds’ blood, which is indicative of relatively recent ingestion of contaminants from the diet. Levels of perfluorinated compounds were exceptionally high, comparable to birds living in highly contaminated sites (such as the Northern American Great Lakes). Some perfluorinated substances were among the highest ever reported in birds, suggesting that Firth of Forth waters and animals are highly contaminated by these man-made substances. Stable isotope results highlighted that in summer there are strong differences in feeding habitat between males and females. GPS positions confirmed these results, showing that males and females visited different areas for feeding. By using information on the type of seabed in these areas, we discovered that females fed mainly in sandy areas, which are a favourable habitat for the small shoaling fish lesser sandeel, whereas males used extensively rocky seabeds, favourable for larger fish species such as the rock butterfish. Variation in location and hence diet between individuals explained their exposure to different types and quantities of chemical contaminants. For example, male shags feeding extensively on large fish found in rocky seabeds have high mercury concentrations in their blood. Critically, we showed that some bodily traits can also be important to determine contaminant levels, even though diet is the main driving factor. By contrast, the differences in diet between individuals could not explain the number of parasites in the stomach of either males or females. This suggests that physiological factors such as the strength of the immune system could better explain the difference in parasite numbers between individual birds. Critically, we showed that the females with the highest numbers of parasites were those having also the highest levels of mercury. This suggests that mercury has a negative effect on their immune defences, and impairs their ability to protect themselves against parasite infections.
Results from this project call for urgent determination of levels of metallic and perfluorinated contaminants in other animals of the Firth of Forth, and the human population. Contaminants can represent a heavy energetic burden to seabirds, because of the cost of detoxification mechanisms. As shown by ECOSEA, heavily contaminated seabirds may be vulnerable to stronger infections of parasites, which in turn constitute an energetic burden and a threat to their health. Through long-term collaboration among ECOSEA partners, we will test the combined effects of contaminants and parasites on energy use, reproduction and mortality on our already available data, and future data collection. Since this shag population is partially migratory, some individuals remain on, or close to, the Isle of May all year long, while others migrate further north on the Scottish coast near Inverness (and other Scottish destinations), where the level of industrial activities and urbanisation is lower than in the Firth of Forth. Individual shags spending the winter at these sites may thus encounter and consume different contaminants than those that stay on the Isle of May. Since we know the winter destinations of the majority of the shags sampled during ECOSEA, we will test the effect of partial migration on contaminant exposure. Identifying when and where seabirds ingest contaminants is extremely valuable in directing efforts towards environmental protection, and sensitise the public to recycling and to careful selection of products and food. Finally, studying the effect of multiple pressures on wildlife is critical to understand observed declines in populations.
European shag