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Monitoring of contaminants and their effects on the common Guillemot and the White-tailed sea eagle

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A main purpose of marine contaminant monitoring in Europe is to evaluate the chemical status and environmental quality under the Marine Strategy Framework Directive (MSFD), to monitor and achieve Good Environmental Status (GES). Characteristics of a good matrix for monitoring purposes are the potential to detect temporal trends or differences between sites or concentration levels in relation to a target value indicating GES. In Sweden we use muscle of herring and eggs of guillemot and White-tailed sea eagle (WTSE) to study changes in contaminant exposure and their effects. Herring is important in fisheries and has target levels set for contaminants in relation to GES. Adult guillemots and eagles in the Baltic Sea are mainly stationary. Guillemots feed largely on herring, WTSEs on fish and other fish-eaters. A higher trophic level may imply biomagnification, and, for example, DDE shows concentration ratios in lipids of 110 (guillemot/herring), 460 (WTSE/herring) and 4.2 (WTSE/guillemot). Banked, frozen guillemot eggs have been extensively used for retrospective temporal trend analyses for several chemicals. Ideally, the matrix should also be useful for biological effect monitoring. Eggshell and reproductive parameters are monitored in the WTSEs and guillemots. Reproductive problems and egg desiccation still occur among eagles, indicating an impact of contaminants and highlighting the importance of apex predators as environmental sentinels.
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A. Bignert and B.O. Helander J Ornithol DOI 10.1007/s10336-015-1240-3
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Monitoring of guillemot and white-tailed sea eagle
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Anders Bignert
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Environmental Research & Monitoring
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Swedish Museum of Natural History
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Bo 50007, SE-104 05 Stockholm, Sweden
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anders.bignert@nrm.se
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Monitoring of contaminants and their effects in the common guillemot and the white-
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tailed sea eagle
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Anders Bignert & Björn O. Helander,
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Dep. Environmental Research and Monitoring, Swedish museum of Natural History
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Bignert 2
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Abstract
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A main purpose in marine contaminant monitoring in Europe is to evaluate chemical status
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and environmental quality under the Marine Strategy Framework Directive (MSFD), to
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monitor and achieve Good Environmental Status (GES). Characteristics of a good matrix for
17
monitoring purposes are potential to detect temporal trends or differences between sites or
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concentration levels in relation to a target value indicating GES. In Sweden we use muscle of
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Herring and eggs of Guillemot and White-tailed Sea Eagle (WTSE) to study changes in
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contaminant exposure and their effects. Herring is important in fisheries and has target levels
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set for contaminants in relation to GES. Adult Guillemots and Eagles in the Baltic Sea are
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mainly stationary. Guillemot feeds largely on Herring, WTSE on fish and other fish-eaters. A
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higher trophic level may imply bio-magnification and e.g. DDE shows concentration ratios in
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lipids of 110 (Guillemot/Herring), 460 (WTSE/Herring) and 4.2 (WTSE/Guillemot). Banked,
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frozen Guillemot eggs have been extensively used for retrospective temporal trend analyses
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for several chemicals. Ideally, the matrix should also be useful for biological effect
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monitoring. Eggshell and reproductive parameters are monitored in WTSE and Guillemot.
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Reproductive problems and egg desiccation still occur among eagles indicating an impact of
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contaminants and highlighting the importance of apex predators as environmental sentinels.
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Keywords: contaminant, desiccation, eagle, egg, guillemot, herring, monitoring, reproduction,
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shell-thickness
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Bignert 3
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Contaminants are measured in a vast variety of sample matrices. Samples from the abiotic
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(e.g. air, water, sediment and sewage treatment sludge) as well as from biological
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environments are collected in large amounts in various monitoring programs around the world
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coordinated by international organizations e.g. UNEP, AMAP (AMAP, 2014), OSPAR
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(OSPAR, 2013), HELCOM. When selecting an appropriate sampling matrix we can set up a
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list of evident criteria that should be fulfilled. These criteria must of course be based on the
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objectives with the program but some general criteria can also be identified.
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The matrix should represent the time and space relevant to the investigation. For air and water
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the exchange rate could be very fast and aggregating samples over a specified period of time.
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Information of the movements of air (back trajectories) and detailed information about
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precipitation and drainage area boundaries may then be necessary to collect in order to define
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what the samples represent. Biological samples represent different time intervals and areas
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depending on the selected specie’s behaviour, home-range, migration, age, trophic level etc.
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Biological samples, unlike abiotic, represents the bio-available fraction of the total
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contaminant load.
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Another important criterion when selecting a sample matrix is the magnitude of the
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unexplained variance. The variance will determine the potential statistical power to detect
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trends or how efficient the measurements will be to show compliance with Quality Standards
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and Good Environmental Status (GES) within the EU, Marine Strategy Framework Directive
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(MSFD).
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In this paper we summarize results from the monitoring of eggshell thickness in common
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Guillemot (Uria alge), eggshell and reproductive parameters in White-tailed sea eagle, also
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referred to as Sea eagle (Haliaeetus albicilla), and of contaminants in Guillemot and Sea
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eagle eggs and in muscle of Herring (Clupea harengus) over more than 40 years. The
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Guillemot feeds on Sprat (Sprattus sprattus) and Herring and has a circumpolar distribution
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(Fig 1 - A). Guillemot breeds in colonies at a number of sites in the Baltic region, with Stora
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Karlsö being the largest breeding colony in the Baltic Sea (Österblom et al. 2002). The
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circumpolar distribution of the Guillemot offers several possible reference sites in remote
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areas. Unlike many other bird species, Guillemot in the Baltic does not migrate far but pass
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the winter in the southern Baltic Proper and is expected to reflect the contaminant situation in
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the Baltic Proper.
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The White-tailed sea eagle is distributed over the Palearctic from Japan in the east to
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Greenland (Nearctic) in the west (Fig 1 - B). Thus, reference sites are available from various
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marine as well as freshwater environments (Jörundsdóttir et al 2009, Riget et al 2010).
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Feeding largely on fish but also on other fish-eaters such as cormorants, mergansers, gulls and
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even seals places this species at the top end of the food web in aquatic environments and
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leaves it highly exposed to persistent and bio-accumulating contaminants. Sea eagles breeding
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on the Baltic coast are commonly resident the year round within their nesting home range and
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thus appear representative for the local/regional environment.
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Breeders of both Guillemot and Sea eagle are faithful to their breeding site through life and
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have a high life expectancy rate, with an observed minimum average annual adult survival in
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the Sea eagle of about 95 % (Helander 2003b). These features enable possibilities for studies
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on effects of contaminants in individual females over time that can illustrate responses to
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temporal changes in contaminant load. It was demonstrated for the first time in Sea eagles on
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the Baltic coast that females exposed to high concentrations of DDTs and PCBs earlier in
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their lives remained sterile after the concentrations in their eggs had decreased (Helander et al.
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2002). Effects possibly linked to contaminants also include decreased eggshell thickness,
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measured in Guillemot and Sea eagle, and egg desiccation, reduced hatching success and
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deformities in embryos observed in Sea eagle.
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Figure 1. The circumpolar distribution of A) the Guillemot and B) the Eurasian
distribution range of the White-tailed sea eagle.
A)
B)
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Methods
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The study areas are outlined in Fig. 2. Since 1968, Guillemot eggs have been sampled from
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Stora Karlsö, 57°17’N, 17° 59‘ E, in the central Baltic Proper for the Swedish National
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Marine Monitoring Program (SNMMP). Sample material from ten eggs are sent for chemical
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analysis each year. Guillemots normally lay just one egg. In case this egg is lost, a
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replacement egg will often be laid. Replacement eggs of guillemot show systematically higher
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concentrations of DDE and sPCB (Bignert et al. 1995). To avoid influence of replacement
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eggs, only early laid eggs are included in the analyses. Early results of brominated flame
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retardants, dioxins and perfluorooctanesulfonic acid (PFOS) are based on retrospective
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analyses of eggs stored frozen in the Swedish National Environmental Specimen Bank
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(further details are given in Miller et al. 2014 and Bignert et al. 1995). The White-tailed sea
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eagle population on the Swedish Baltic Sea coast has been surveyed annually since 1964 and
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inland populations since 1976 (Helander 2003a). Dead eggs have been saved from the nests
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continuously over the years for investigation (Helander et al. 1982, 2002, 2008), since 1989
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within the (SNMMP). Sampling of Herring for monitoring purposes started at two sites 1972
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and has been enlarged several times and comprises at present around 20 sites along the
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Swedish coast that are sampled at least once a year.
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Figure 2. Study areas in the Baltic Sea. The sampling sites for Herring used in this study, is
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Utlängan (1) in southern Baltic Proper, sampled since the 1970s, Landsort in northern Baltic
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Proper (2) and Ängskärsklubb (3) in southern Gulf of Bothnia. The Guillemot sampling site is
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Stora Karlsö, central Baltic Proper (red dot). White-tailed sea eagle was sampled along the
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Swedish coast of the Baltic Proper (BP) and Gulf of Bothnia (GB) (green areas).
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Spring caught Herring from Karlskrona archipelago and Ängskärsklubb, about 200 km SW
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and 350 km N, respectively, from the Guillemot colony at St Karlsö, and autumn caught
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herring at Landsort (2) about 200 km N, was used for comparisons Sea eagle/Guillemot and
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Herring. Sampling and preparation of herring muscle have been presented earlier, as well as
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reasons for the choice of sampling locations, size and age classes used within the monitoring
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program (Bignert et al., 1998). Herring muscle tissue, compared to several other fish species,
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is relatively rich in lipids, and hence useful for analyses of lipid-associated contaminants.
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The preparation of samples for analyses was conducted at the Swedish museum of Natural
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History. Eggs were weighed to the nearest 0.01 g, measured (length and width) to the nearest
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0.01 mm and rinsed externally with tap water before being opened. Eggs with no or small
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embryos were emptied into a sterile glass jar through a hole drilled at the equator; in eggs
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with larger embryos the hole was enlarged with tweezers. Egg contents were homogenized
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and a 5-10 g aliquot was taken out from each egg for analyses. Embryo length was recorded
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before homogenization. The inside of the egg shell was rinsed clean with tap water and the
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shell then left to air-dry in room temperature. The weight of the dry shell was recorded and
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the eggshell-thickness was measured at the equator using a modified Starret 1010 dial
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micrometer. Eggshell thickness was also measured with the same equipment in eggs from the
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Baltic coast 1856-1935, saved in museum and private collections. This sample, dating from
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before the introduction of DDT in the 1940s, was used as reference for comparison with the
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recent samples.
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A desiccation index (Di) based on the weight of sampled egg´s content in relation to inside
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egg volume was introduced in order to measure the degree of dehydration of the egg: Di=(W-
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S)/V where W=total weight of the sampled egg, S=dry shell weight and V=inside egg volume
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as calculated by a formula given by Stickel et al. (1973) with adjustment for eggshell
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thickness to give the inside volume (Helander et al. 2002). Di is high in a normal egg
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(theoretical maximum 1.0) and decreasing when the egg gets desiccated. Our dead eggs were
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generally collected within four to eight weeks after normal hatching time and an estimate of
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an approximately “normal” Di in such eggs ranged down to ca. 0.70.
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Based on the frequency distributions of occupied nests containing 0, 1, 2 or 3 nestlings, three
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reproductive parameters are followed annually for the White-tailed sea eagle. Breeding
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success denotes the proportion of reproducing pairs in the population, nestling brood size is
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the mean number of young produced per successful breeding, and productivity denotes the
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mean number of young produced per checked territorial pair in the population. Brood sizes
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are calculated as arithmetic means with 95 % confidence intervals assuming normal
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distribution. The surveys are performed in two steps during the breeding season. Nest-
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occupancy is determined in April from aerial surveys or distance observations. In May-June
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all occupied nest are revisited and inspected to assess the reproductive outcome. To avoid a
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bias caused by nestlings lying down and invisible from the ground, mean brood size should be
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assessed only from nests that were climbed to, or otherwise verified from the same level. For
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assessments of possible impacts from contaminants on reproductive parameters, information
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from a supposedly unaffected population is useful for reference. To estimate such background
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reference values we used data assembled from the Swedish coastal eagle population: nestling
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brood size records from 1854-1950, and sets of breeding success data comprising from three
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to ten years in succession from eight eagle territories, 1915-1953 Helander 1994a, Helander et
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al. 2003a). An estimate for productivity was derived by combining the data for breeding
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success and brood size. These data indicated no change up to the end of the time periods and
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thus no significant impact of contaminants so far.
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To study relationships between reproduction and contaminant loads in the White-tailed sea
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eagle, residue concentrations in analysed eggs were related to productivity (the mean number
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of young produced per year) of the eagle territory over a 5-year period, consisting of the egg-
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sampling year ± 2 years (Wiemeyer 1984, 1993, Helander 1994b). Years when breeding
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attempts failed after human disturbance at the nest, and years when sub-adults occurred in the
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mated pairs resulting in no egg production, were excluded from the calculations of
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productivity. If the 5-year period around a sampling year overlapped with another 5- year
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period around a sampling year representing the same female, a mean value for productivity
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was calculated over the period from the first egg-sampling year 2 years to the last egg-
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sampling year +2 years, and a mean value for each contaminant was calculated from all
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clutches within that period. This was done to avoid an over-representation of a few females in
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the sample (Helander et al. 2002). In most cases the 5-year productivity represented the same
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individual female. Continuity and turnover of individuals in the territories was based on field
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observations, the characteristics of moulted feathers (Rüger & Neumann 1982, Struwe-Juhl &
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Schmidt 2002) and the reading of rings on the birds.
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Chemical analyses of organic contaminants presented here have been reported in various
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articles referred to in the text and were carried out at Stockholm University (SU). The first
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mercury analyses in Guillemot were carried out at the Royal Institute of Technology, 1968-
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1974, thereafter at Swedish University of Agricultural Sciences (SLU) in 1975 2006 (with a
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few missing years) and from 2007 and onwards at SU. In herring, mercury was analysed at
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SLU, 1972-2006 and from 2007 at SU. Total-mercury concentrations are given on a fresh
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weight basis. In fish and bird eggs total-mercury is predominantly in the form of methyl-
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mercury (Kamps et al. 1972, Ackerman et al. 2013).
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Many of the contaminants monitored are lipophilic substances and are thus stored in the body
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lipids in biota, and concentrations are here given on a lipid weight basis. Lipid content from
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Guillemot eggs is consistently high and stable (yearly mean for > 40 years, ~12%) compared
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to that of herring (yearly mean for > 20 years, ~3%). Lipid content in 40 Sea eagle eggs
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averaged about 4.55 % [S.E. 0.23] (Helander et al. 1982). PCB concentrations in eagle eggs
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are given as total-PCB, calculated according to Helander et al. (2002), also in Guillemot and
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Herring calculated according to Bignert et al. (1998). Geometric yearly mean values have
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been used for trend estimates when all available contaminant measurements were from
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individual specimens (e.g. in Table 1 below). When a mixture of results from pooled samples
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and individuals have been used, arithmetic means have been applied (e.g. in Fig. 3). Temporal
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trends in the current study have generally been shown as 5 or 7 years running mean
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smoothers, provided they can explain significantly more of the variation in concentrations
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compared to linear regression, this is tested by means of Analyses of Variance according to
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Nicholson et al. (1998). Chemical substances included in this presentation are
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dichlorodiphenyltrichloroethane (DDT), Dichlorodiphenyldichloroethylene (DDE), total sum
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of polychlorinated biphenyl’s (PCB), Polychlorinated biphenyl IUPAC 153 ([P]CB-153),
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Hexachlorocyclohexanes (α,βand ɤ HCH), [lindane]), Hexachlorobenzene (HCB), ,
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Hexabromocyclododecane (HBCDD), perfluorooctane sulfonate (PFOS) and total-mercury
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(Hg).
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Results
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Temporal trends of contaminants
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The temporal development of DDE, (P)CB-153, S-TCHD, total-Hg, (P)BDE-99, (P)BDE-47,
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HBCDD and PFOS are illustrated in Fig 3. Several of the classical very persistent organic
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contaminants show a clear and significant decreasing trend (Fig 3A), whereas the trends in
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Fig. 3B show a marked increase for PBDEs during the 1970s followed by a decrease from the
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mid-1980s, and marked increases from the 1970s until about 2005 and decreases thereafter for
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HBCDD and PFOS.
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Figure 3. Temporal development of contaminants in Guillemot eggs in Sweden. A) Total
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mercury (Hg), dioxins and furans (sTCDD), PCBs (CB-153) and DDE. B) Brominated flame
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retardants (BDE-47 and BDE-99) and perfluorooctane sulfonate (PFOS). (Figures drawn from
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data in Bignert et al 2014b, Sellström et al. 2003 and Holmström et al., 2005).
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The decreasing trends of DDE in Guillemot and White-tailed Sea eagle eggs are
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approximately congruent with the corresponding trends in herring (Fig 4). A somewhat earlier
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and steeper decline can be shown in the Baltic Proper in Guillemot, Sea eagle and Herring
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compared to the Bothnian Sea (WTSE and herring). The increase of DDE in first seen in
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herring from s. Baltic Proper in the mid 80ies has been interpreted as an effect of a DDT
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campaign in former East Germany (Bignert et al., 1998). A delayed response can possibly be
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reflected in the time series of guillemot, WTSE and also in herring from the s. Bothnian Sea
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(Fig 4).
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Figure 4. DDE concentrations expressed as percent of the concentration measured in the year
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1972. Congruent development of DDE in Guillemot, White-tailed Sea eagle and Herring from
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the Bothnian Sea and the Baltic Proper
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Despite the strong decrease of DDE in Guillemot eggs in the Baltic (Fig 3A) the
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concentrations are still much higher than in guillemot eggs from colonies in the north Atlantic
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(Fig 5).
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Figure 5. Concentrations of DDE in Guillemot eggs at Stora Karlsö in the Baltic Sea and in
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colonies in the North Sea. Green indicates 0-2, yellow 2-4, and red more than 4 ug/g l.w.
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Figure drawn from data in Jörundsdóttir et al. (2009)
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The ability to detect trends for monitoring purposes depends on the statistical power of the
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time-series. A minimum required power to detect trends was set to 80%. From that criterion,
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minimum detectable trends for a monitoring period of 10 years for various analyzed
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substances both in Guillemot egg and Herring muscle were estimated (Table 1). The results
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show that for several of the included, very persistent substances, the Guillemot performs
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better compared to the Herring in terms of improved sensitivity to detect trends. For CB-153,
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DDE, HCB, dioxins (TCDD- equivalents) and HBCD the Guillemot time-series can detect
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about half of an annual change or less, compared to the Herring time-series.
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Substance
n
Guillemot
(% / yr)
Herring
(% / yr)
CB-153
17
6.8
18
DDE
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6.5
14
α -HCH
15
8.3
6.5
β-HCH
15
2.6
6.9
ɤ -HCH
15
*
6.3
HCB
16
6.3
16
HBCD
6
7.3
13
TCDD-Eqv
13
3.7
7.2
Tot-Hg
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6.1
7.5
Table 1. Minimum detectable trend (% per year) during a sampling period of 10 years with a
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power of 80 % in Guillemot eggs and Herring muscle, from Utlängan i.e. a lower percentage
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implies that the time-series are more likely to detect a present smaller trend. The estimates are
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based on data from the last 10 years of monitoring. * ɤ -HCH was below level of
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quantification the last 10 years.
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Bio-magnification of contaminants
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A higher trophic level may imply bio-magnification in the concentrations of contaminants. In
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Table 2, relative concentrations of seven studied organic contaminants and total
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mercury(predominantly methyl-mercury) show higher concentrations in Sea eagle and
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Guillemot eggs compared to Herring (Table 2). A high biomagnifications may enable
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chemical analysis at low environmental concentrations and hence improve the statistical
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power to detect differences or trends. The ratios of concentration between various monitoring
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indicators may give valuable information for the evaluation of measured concentration in
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relation to Quality Standards.
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Substance Guillemot Sea eagles
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PCB 17 400
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DDE 110 460
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a-HCH 0.7 4.5
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b-HCH 20 72
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ɤ -HCH 0.68 (1.4)
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HCB 31 17
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Hg 15 (N.m.)
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Table 2. Concentrations in Guillemot and Sea eagle egg relative to the concentrations in
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Herring muscle from Landsort, median ratios for 2000-2013. (N.m.) = not measured
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Observed effects and trends
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Eggshell thickness. Shell thickness in relation to DDE in egg content in Guillemot and Sea
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eagle eggs is outlined in Fig. 6. The relationships are non-linear, with most of the effect
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showing at the lower end of the range of concentrations, especially for the Guillemot. Shell
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thickness of Guillemot eggs 1969-1974 was approximately 10 % thinner than in a reference
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sample from 1861-1934 (n=45). The mean eggshell thickness in whole Sea eagle eggs
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retrieved on the Baltic Sea coast 1965-1974 was 18 % thinner than in the reference sample
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from 1856-1935. Shell-thinning was not correlated with concentrations of PCB but was
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significantly correlated with DDE and an estimated threshold level of 30-50 µg/g l.w. [~ 1.5-
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2.5 µg/g w.w.] was implied (Helander et a. 2002). The shell thickness in individual Sea eagle
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eggs 2000-2010 (n=183) was still 6 % thinner than in the pre-1940 reference sample (n=109)
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(p<0.001).
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Figure 6. Eggshell thickness in relation to concentrations of DDE in 439 Guillemot eggs
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(1969-2012) and 385 White-tailed sea eagle (WTSE) eggs (1965-2012) in Sweden. The
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individual measurements have been grouped in concentration intervals and only the mean
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concentration for each group (19 and 15 groups, respectively) is shown in the figure. The
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eggshell thickness shows a significant decrease with increasing concentrations of DDE in
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both Guillemot (r2=0.25, p<0.029) and WTSE (r2=0.73, p<0.001)
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Egg desiccation. Calculated Di-values of individual eggs are plotted in relation to the
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concentrations of DDE and PCB in the egg contents in Fig.7. An effect threshold level at 170
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µg/g DDE and/or 1000 µg/g PCB is indicated, and at concentrations exceeding 500 µg/g DDE
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or 2000 µg/g PCB all eggs had Di-values below 0.70 (the estimated threshold for a “normal”
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egg). Fig. 8 illustrates temporal changes in the occurrence of desiccated eggs and
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concentrations of DDE in egg contents over the study period. Eighty-six % of the eggs
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collected 1965-1991 had Di-values below the estimated threshold of 0.70, with 58 % as low
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as 0.15 - 0.50. During 1992-2008 the situation had improved: only 19 % with Di-values below
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0.70 and 2 % in the range 0.30 - 0.50. Desiccated eggs (Di = 0.17 0.57) with very high
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concentrations of DDE and PCBs have again occurred in 2009-2013 among a few females on
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the northern Baltic coast.
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Figure 7. Desiccation of White-tailed sea eagle eggs in relation to concentrations of DDE and
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PCB in the egg contents. An effect threshold level is implied at 170 µg/g DDE and/or 1000
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µg/g PCB and at concentrations exceeding 500 µg/g DDE and/or 2000 µg/g PCB all eggs had
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Di-values below 0.70 (Redrawn from Helander et al. 2002).
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Figure 8. Temporal changes in concentrations of DDE in egg content in relation to desiccation
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index in White-tailed sea eagles on the Swedish Baltic coast, 1965-2013. Red dots indicate
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mean concentrations of DDE and small black dots indicate individual Di-values; the red line
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indicates the log-linear regression line for DDE and the blue line indicates the connected
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annual mean desiccation indices. Note the occurrence of desiccated eggs again in recent years.
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Reproduction. The temporal trend in breeding success 1964-2013 in the Baltic Proper and in
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the Gulf of Bothnia is outlined in Fig. 8. The estimated reference level for this parameter is 72
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% with 95 % C.I. 59-86 %. The breeding success was deeply depressed but improved strongly
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during the 1990s, to level off within the confidence interval of the reference level from the
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late 1990s.
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Figure 9. Breeding success of White-tailed sea eagles on the Swedish coast of the Baltic
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Proper (left) and Gulf of Bothnia (right), 1964-2013. The smoothed lines represent 7-years
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running mean values. The yellow strip indicates the 95 % confidence interval round about an
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estimated reference level (Helander 2003a).
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Hatching failure can include the full clutch and then affects the breeding success, or be partial
354
and be seen as a reduction of the mean nestling brood size in successful nests. Temporal
355
trends in nestling brood size are shown in Fig. 10. A strong decrease occurred already in the
356
early 1950s and continued to a bottom level during 1966-1985. Nestling brood size has
357
improved after that but appears to have stabilized below the reference background level. This
358
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is mainly due to a situation in the Gulf of Bothnia where the mean brood size remains
359
significantly smaller than the background level. This can be linked to a higher frequency of
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dead eggs in nests containing young (2000-2009): 7.1 % in the Gulf of Bothnia (n=461
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checked nests) as compared to 2.9 % in the Baltic Proper (n=932 checked nests) (p<0.001).
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Figure 10. Temporal distribution of nestling brood size of White-tailed sea eagles on the
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Swedish Baltic coast, 1854-2013. The grey-shaded strip is the 95 % confidence interval
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around a mean background reference level (1.84) based on data from ringers and literature
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from before 1951 (Helander 1994a, 2003a).
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The net result of breeding success and nestling brood size is seen in the productivity. In
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Figure 11 the mean productivity over a 5-year time period centered round about a sampling
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year for an analyzed egg from each of 82 females is used in relation to concentrations of DDE
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and PCB in the eggs (see Methods for details). The data are grouped into concentration
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intervals for DDE and PCB, and the corresponding mean productivity of the females within
375
each concentration interval is indicated. For DDE, an S-shaped dose-response curve is
376
implied, with a first effect as concentrations exceed 100 µg/g, an inflection point at ca 210
377
17
µg/g and zero reproduction as concentrations exceed 900 µg/g (Fig. 11). For PCB the curve
378
implies a more linear relationship, with zero reproduction at 2000 µg/g. The correlations are
379
highly significant for both DDE and PCB (p<0.001).
380
381
382
383
384
Figure 11. Mean five-year productivity of 82 White-tailed sea eagle females grouped into
385
concentration intervals for DDE and PCB in their eggs. (Redrawn from Helander et al. 2002).
386
387
388
389
390
391
18
392
Figure 12. Temporal changes in concentrations of DDE and PCB in egg content in relation to
393
productivity in White-tailed sea eagles on the Swedish Baltic coast, 1965-2013. The blue dots
394
indicate mean concentrations of DDE with 95 % confidence intervals, the jagged line shows
395
the annual productivity. The green, upper line indicates the estimated pre-1950s reference
396
level for productivity of Baltic Sea eagles and the yellow area indicates its lower 95 %
397
confidence limit. The improvement in productivity is largely mirrored in the desiccation index
398
in Fig.7.
399
400
401
19
Discussion
402
Various criteria can be listed to determine the appropriateness of environmental contaminant
403
indicators. If trend detection is an important objective, it is an advantage if the random
404
unexplained variation can be kept as low as possible. The statistical power to detect trends
405
improves with increasing sample sizes and length of the study period, but decreases with
406
increasing random between-year variation (Bignert et al. 2004). In a comparison between
407
Herring and Guillemot, the sensitivity to detect trends, expressed as the minimum trend (%
408
per year) possible to detect with a statistical power of 80% over a monitoring period of 10
409
years with annual sampling was estimated (Table 1). For many of the studied contaminants,
410
considerably smaller trends were possible to detect with Guillemot eggs compared to the
411
Herring muscle (Table 1). Higher contaminant concentrations due to bio-magnification can
412
lower the chemical analytical error. But more important may be the fact that the predator eats
413
a lot of fish leading to a similar effect as when pooling of individual samples reduces the
414
biological variation, which is generally substantially higher than the variation due to the
415
uncertainty of chemical analysis (Bignert et al. 2014a). For α-HCH and ɤ -HCH no bio-
416
magnification takes place and the concentrations (lipid weight basis) were actually lower in
417
guillemot than in herring (Table 2). The ɤ-HCH concentrations in guillemot eggs have even
418
been below the limit of quantification during the most recent 10 years. For β-HCH that has 20
419
times higher concentrations in Guillemot compared to Herring (Table 2), the possibility to
420
detect smaller trends is much better in Guillemot than in Herring.
421
422
The observed magnification in this study of some concentrations on a lipid weight basis from
423
Herring to Guillemot eggs is similar to the magnification of concentrations on a fresh weight
424
basis reported from fish to Osprey Pandion haliaetus eggs (Henny et al. 2003). For DDE and
425
totalPCB, they reported bio-magnification ratios of 87-156 and 11-20, respectively, compared
426
to 109 and 17 in this study. Both these species are obligate fish-eaters. The White-tailed Sea
427
eagle is not feeding on Herring but on other fish-eaters including pike Esox Lucius, Perch
428
Perca fluviatilis and mergansers Mergus spp., cormorants Phalacrocorax spp. and gulls Larus
429
spp. and is thus at a higher trophic level, as indicated from the concentration ratios in Tab 2.
430
A considerable difference can be noted between Guillemot and Sea eagle in ratios for the
431
studied substances. Based on the ratios for the predators in relation to Herring in Tab 2, a
432
biomagnification of 4.2 for DDE is implied from Guillemot to Sea eagle, compared to 23 for
433
PCB in this dataset. When Guillemot is compared with autumn caught Herring from the
434
20
northern Baltic Proper (Fig.2, area 2), as reported in Tab 2, the average DDE-ratio (110)
435
differs considerably from the PCB-ratio (17). If instead the average DDE- and PCB-ratios
436
between Guillemot and spring caught Herring from the southern Baltic Proper (Fig.2, area 1)
437
are calculated, the ratios are similar, around 50. This may indicate that the Guillemot feeds on
438
Herring closer to the southern Herring population. For α-HCH, β-HCH and HCB
439
biomagification in the range 2 - 6 is implied between Guillemot and Sea eagle whereas no
440
biomagnification is indicated for ɤ -HCH in the chain Herring-Guillemot-Sea eagle.
441
442
Bird eggs are used in monitoring projects from various parts of the world (e.g. Dittmann et al.
443
2012, Nordlöf et al. 2010, Johansson et al. 2011). Contaminant analyses of Guillemot eggs
444
(Fig.3), collected annually for more than 40 years, have proven useful for studies of a number
445
of old well-known substances as well as for retrospective analyses of emerging substances
446
from eggs stored frozen in the Swedish National Environmental Specimen Bank (Lundstedt-
447
Enkel et al., 2006, Bignert et al., 2014b). As illustrated in Fig.4, the temporal trends are most
448
often parallel to trends in their feed, or in other biological matrices (or e.g. in sediment,
449
Olsson et al., 2000) but less variable implying a higher statistical power to detect trends.
450
Trends of DDE, PCB, dioxins and furans, and mercury show that measures to eliminate or
451
reduce discharges has been efficient, that new threats (e.g. brominated and fluorinated flame
452
retardants and surfactants) can be disclosed (Sellström et al., 2003, Holmström et al., 2005),
453
and thus support bans of persistent substances with adverse effects on wildlife and humans.
454
However, despite the banning of DDT in the 1970s and the decrease in DDE concentrations
455
over time since then, the concentrations are still very much elevated in the Baltic compared to
456
the North Sea, as illustrated from analyses of Guillemot eggs (Fig.4).
457
458
Eggshell thickness is known to decrease at exposure of DDE in some birds (e.g., Cooke 1973,
459
Peakall and Lincer 1973, Lincer 1975, Lundholm 1997). Our results imply that the Guillemot
460
seems to be less sensible to DDE for eggshell thinning than the Sea eagle. Another alcid in the
461
Baltic Sea, the Razorbill Alca torda, in 1970-1972 had concentrations of DDTs and PCBs in
462
their eggs in the same range as Sea eagles but shell thinning was 50 % higher in the eagle
463
eggs (Andersson et al. 1974, Helander et al. 2002). No effect was observed on reproduction in
464
Razorbills (Andersson et al. 1974), at concentrations where Sea eagle reproduction was
465
reduced by near 80 % (Helander et al. 2008), a striking example of differences between
466
species in response and vulnerability to chemical pollutants. There was no significant
467
correlation between Sea eagle productivity and eggshell thickness of whole eggs (Helander et
468
21
al. 2002). Eggs that break due to thinning or other structural changes in the shell would of
469
course affect productivity, but it can often not be judged whether egg breakage was caused by
470
predators or was a result of changes in the shell itself.
471
472
A remarkable feature during the 1960s and through the 1980s among eagles on the Swedish
473
Baltic Sea coast was a high occurrence of desiccated eggs in the nests. Strong correlations
474
were found between Di and productivity, and with Di and DDE and PCBs, but not with
475
eggshell thickness (Helander et al. 2002). The correlation was higher for DDE than for PCB
476
but the strong co-variance in DDE and PCB concentrations made further interpretations
477
difficult. As DDE in the eggs decreased below the suggested effect threshold level around
478
1990 a strong improvement followed in eggshell quality, as expressed by the mere absence of
479
desiccated eggs during the 1990s (Fig.8). Mean PCB concentrations in the eggs, however, did
480
not decline below the implied possible threshold level of 500 µg/g (Fig.7) until the late 1990s
481
(Fig.12), implying that the suggested possible effect from PCB on eggshell quality (Fig.7)
482
was probably a result of covariance with DDE. The recent occurrence of desiccated eggs
483
among a few females on the northern Baltic coast with very high concentrations of DDE and
484
PCBs in their eggs indicates that there are still high enough concentrations in biota to cause
485
concern.
486
487
In studies of effects, the strong inter-correlation between DDE and PCB concentrations in the
488
eggs often makes it difficult to distinguish possible effects between the two (Helander et al.
489
1982, 2002). In all except one of our attempts so far to study effects in the Sea eagle, the
490
correlation has been stronger for DDE. The exception was for embryo toxicity where the load
491
of PCB (represented by CB-138) but not DDE was significantly higher in eggs with dead
492
embryos, implying the possibility of embryo mortality at concentrations of totalPCB of 500
493
µg/g (Helander et al. 2002). Deformities in Sea eagle embryos have been observed
494
occasionally over the study period. Observed deformities include neck oedema, cross-bills
495
and toe deformities. Such features have been reported for other species including eagles and
496
connected with effects from dioxins and coplanar PCBs (e.g. Grier 1968, Gilbertson et al.
497
1976, 1991, Bowerman et al. 1994, Giesy et al. 1994) and may have been more frequent in
498
Baltic Sea eagles when the concentrations of PCBs were higher. Before the 1990s, egg
499
contents were often in a stronger state of decay than in more recent eggs, possibly connected
500
to the poorer eggshell quality making those eggs more susceptible to bacterial infection. The
501
possibilities to detect abnormal features in the rotting embryos were then small and often not
502
22
even possible. Examples of deformities observed in White-tailed sea eagle embryos are
503
illustrated in Figure 13.
504
505
506
Figure 13. Neck oedema, toe deformities and
507
crossbills observed in Swedish White-tailed sea eagle embryos and nestling. Photos
508
B.Helander
509
510
511
After the mid-1980s there was a clear decrease in the occurrence of desiccated eggs (Fig 8)
512
followed by an increase in productivity (Fig 12). Productivity was even more strongly
513
correlated to Di than to DDE, the proposed causative agent for the structural changes leading
514
to excess desiccation; a plausible explanation for this was that many females that had been
515
exposed to high concentrations of DDTs and PCBs continued to lay eggs that dried out and
516
remained unproductive throughout their lives, despite the fact that the concentrations of these
517
contaminants decreased in their eggs to levels at which other, younger females reproduced
518
successfully (Helander et al. 2002). As these old, sterile females were phased out from the
519
population the mean annual productivity could rise faster, as seen during the 1990s. In the
520
population as a whole the productivity stabilized at a near-normal level from the mid- to
521
late1990s.
522
523
23
Poor reproduction and a decreasing White-tailed sea eagle population in the early 1960s was
524
the first obvious signal for effects of harmful chemicals in the Baltic Sea. This was in a time
525
of dawning awareness of environmental issues after the publication by Rachel Carson of her
526
classic “Silent Spring” (1962). Retrospective studies later showed that a significant drop in
527
sea eagle nestling brood size occurred in the Baltic population already in the early 1950s
528
(Helander 1985, and Fig. 10). Despite the strong improvements observed in eggshell and
529
reproductive parameters in this species in the Baltic, the significantly smaller nestling brood
530
size, higher rate of dead eggs and re-occurring incidence of desiccated eggs observed in the
531
Gulf of Bothnia, and the prevailing significant egg-shell thinning in the coastal Sea eagle
532
population, still indicate a serious state of the Baltic environment..
533
534
Conclusion
535
Birds and bird eggs have proved to be efficient bio indicators both for contaminant trend
536
analyses and for the deleterious effects caused by contaminants. In the Baltic, decreasing
537
trends of several classical contaminants such as mercury, dioxin, sPCB and DDE have
538
decreased to approximately 40, 30, 5 and less than 5 percent of their peak concentrations in
539
the beginning of the 70’ies along with a recovery from adverse effects caused by them can be
540
clearly shown. Bird eggs, often but not always, perform better to detect trends than fish
541
possibly partly due to their “pooling” of many fish. Birds at higher trophic levels are more
542
prone to be affected by contaminant than e.g. fish through bio-magnifications.
543
544
545
Acknowledgements
546
We would like to thank the Swedish EPA for ongoing funding for the SNMMP. Thank you
547
also to the various field and laboratory personnel who have helped in collecting and preparing
548
materials for analysis over the many years the SNMMP has been running. All sampling was
549
performed with legally necessary permits.
550
551
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... Even after some compounds are banned, such as PCBs or polybrominated diphenyl ethers (PBDEs), new chemicals are produced to replace the regulated ones (Stockholm Convention, 2009). Many of the anthropogenic as well as some of the natural compounds, for example, PBDEs, are harmful to the environment, and have been proven to cause health problems in exposed species (Bignert and Helander, 2015;Cervin et al., 2020;Roos et al., 2012;Sonne et al., 2020;Wolkers et al., 2000). ...
... Retrospective analyses of samples from environmental specimen banks (ESBs), also known as time-trend studies, are frequently used to track the effect of regulations or bans of harmful chemicals. In most time-trend studies, a targeted approach has been used to disclose trends for certain contaminant groups, such as fluorinated compounds (Holmström et al., 2005;Huber et al., 2012;Miller et al., 2014;Roos et al., 2014), brominated contaminants (Roos et al., 2014;Stapleton et al., 2006) or, most frequently, persistent organic pollutants (POPs), such as PCBs, DDTs, and hexachlorocyclohexanes (Aguilar et al., 2002;Bignert and Helander, 2015;Bignert et al., 1998;Holmström et al., 2005;Jensen et al., 1972;Jeong et al., 2020;Miller et al., 2014;Norstrom et al., 1988;Nyberg et al., 2015;Olsson et al., 2019;Roos et al., 1998;Roos et al., 2012;Roos et al., 2014;Sun et al., 2020). The levels of legacy POPs in the Baltic Sea ecosystem have been shown to have declined after international restrictions were introduced in 1970-80s (AMAP, 2017;Muir and Howard, 2006), leading to improvements in the health of Baltic top consumer species (Roos et al., 2012). ...
... The choice of the key top consumer species for investigation was based on ecological relevance, well-established pollutant-linked health problems, and availability of archived tissue samples in the Swedish environmental specimen bank (ESB) (Bignert and Helander, 2015;Cervin et al., 2020;de Wit et al., 2020;Roos et al., 2012;Sonne et al., 2020). The following predator tissue samples were investigated: harbor porpoise (Phocoena phocoena) blubber , common guillemot (Uria aalge) eggs , and white-tailed sea eagle (Haliaeetus albicilla) muscle . ...
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The rate of decline in regulated persistent organic pollutant (POP) concentrations in Baltic Sea biota has leveled off in recent years, with new contaminants frequently being discovered. There is, therefore, a need for comprehensive approaches to study occurrence and temporal trends of a wide range of environmental contaminants, including legacy POPs, contaminants of emerging concern (CECs), and new contaminants. In the current work, non-target screening (NTS) workflows were developed and used for, to the best of our knowledge, the first time-trend directed NTS of biota using gas chromatography–high-resolution mass spectrometry (GC-HRMS). To maximize contaminant coverage, both electron ionization (EI) and electron capture negative ion chemical ionization (ECNI) were used. The EI data were treated using highly automated workflows to find, prioritize, and tentatively identify contaminants with statistically significant temporal trends. The ECNI data were manually processed and reviewed prior to time-trend analysis. Altogether, more than 300 tentatively identified contaminants were found to have significant temporal trends in samples of Baltic guillemot, harbor porpoise, or white-tailed sea eagle. Significant decreases were found for many regulated chemicals, as could be expected, such as PCBs, polychlorinated terphenyls, chlorobenzenes, toxaphenes, DDT, other organochlorine pesticides, and tri- and tetra- bromodiphenyl ethers (BDEs). The rate of decline of legacy POPs agreed well with data reported from targeted analyses. Significant increases were observed for small polycyclic aromatic hydrocarbons, heptaBDEs, CECs, and terpenes and related compounds. The CECs included, among others, one plasticizer tributyl acetylcitrate (ATBC), two antioxidants 2,6-bis(1,1-dimethylethyl)phenol and 2,6-bis(tert-butyl)-4-(4-morpholinyl-methyl)phenol, and two compounds used in polymer production, trimethyl isocyanurate and 2-mercaptobenzothiazole, which had not previously been reported in biota. Their increased concentrations in biota indicate increased use and release. The increase in ATBC may be linked to increased use of it as a substitute for di-2-ethylhexyl phthalate (DEHP), which has been phased out over the last decade.
... However, the eggshell thickness was still signicantly correlated with DDEs levels in the eggs of the common guillemot and whitetailed eagle (p < 0.029 and 0.001, respectively). 33 Miljeteig 73 analyzed the eggshell of the ivory gull in the Arctic, and their results suggested that OCPs and PBDEs were correlated with the shell thickness (p < 0.021), which was still thinner than that in the 1930s. The hatching success (77%) of tree swallow from a dioxin-polluted area was lower compared with that (85%) in the reference sites from Rhode Island, USA. ...
... Developmental deformities of the beak, head and feet have been reported in many sites. 19,20,33 These deformities can comprise individual tness and survival, for instance, beak deformity can lead to dietary changes and reduced foraging success. An in ovo experiment demonstrated that exposure to 0.25 ng g À1 PCB-126 can result in various types of deformities in chicken, including neck and head edema, foot or leg deformity, and gastroschisis and hip dysplasia. ...
Article
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Within the context of explosive growth of persistent organic pollutants (POPs) list, the scientific community is combatting the increasing challenges of protecting human and wildlife from the potentially negative consequences...
... This high contamination has been associated with detrimental effects on seals in terms of impaired reproduction and histopathological damage, leading to severe population impacts (Bergman, 2007;Bergman and Olsson, 1985;Blomkvist et al., 1992;Harding et al., 2007;Helle et al., 1976a,b;Olsson et al., 1975;Routti et al., 2005Routti et al., , 2008Routti et al., , 2009). In addition, in seabirds, birds of prey and fish, a plethora of harmful health effects has been reported (Gercken et al., 2006;Skarphedinsdottir et al., 2010;Bignert & Helander 2015, Helander et al., 1982, 2002. Although efforts have been made to quantify population level effects following reports of multiple health effects on Baltic sentinel species, there is a grave lack in efforts to quantify risks of population effects in fish and invertebrates, such as bivalves (Korsman et al. 2012;Roos et al., 2012;Helander et al., 2008;Siebert et al., 2006Siebert et al., , 2007HELCOM, 2010HELCOM, , 2018. ...
... Most eggs concentrations fell within the LRC (98.1%), and the remaining 1.9% belonged to the MRC. While none of the measured eggs signified no risk for foetus, there was also a general lack of individuals in the higher RCs, likely due to the overall decrease in Hg contamination observed in common guillemot within the Baltic Proper (Bignert and Helander, 2015). These declines corresponded well with the declines in Hg in body feathers of whitetailed eagles (Sun et al., 2019) and are in agreement with observations made by Rigét et al. (2011) for decreasing Hg time trends towards the Scandinavian regions. ...
Article
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A wide range of species, including marine mammals, seabirds, birds of prey, fish and bivalves, were investigated for potential population health risks resulting from contemporary (post 2000) mercury (Hg) exposure, using novel risk thresholds based on literature and de novo contamination data. The main geographic focus is on the Baltic Sea, while data from the same species in adjacent waters, such as the Greater North Sea and North Atlantic, were included for comparative purposes. For marine mammals, 23% of the groups, each composing individuals of a specific sex and maturity from the same species in a specific study region, showed Hg-concentrations within the High Risk Category (HRC) and Severe Risk Category (SRC). The corresponding percentages for seabirds, fish and bivalves were 2.7%, 25% and 8.0%, respectively, although fish and bivalves were not represented in the SRC. Juveniles from all species showed to be at no or low risk. In comparison to the same species in the adjacent waters, i.e. the Greater North Sea and the North Atlantic, the estimated risk for Baltic populations is not considerably higher. These findings suggest that over the past few decades the Baltic Sea has improved considerably with respect to presenting Hg exposure to its local species, while it does still carry a legacy of elevated Hg levels resulting from high neighbouring industrial and agricultural activity and slow water turnover regime.
... In the Swedish coast of the Bothnian Sea, the levels of PCB and DDT along with other POPs in white-tailed eagle eggs are elevated compared to the rest of the Baltic Sea. This coincides with decreased productivity of the eagles nesting in this area (Bignert and Helander 2015;Hellström 2015). ...
Thesis
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Apex predators regulate ecosystems through top-down processes. In the last century many predator populations crashed due to anthropogenic impacts, but recently some have recovered and are re-colonizing old areas, as well as expanding to new suitable habitats. Rapid loss or return of apex predators can destabilize ecosystems and cause consequences for their prey species as well as for livestock. In the Baltic Sea area, the white-tailed eagle (Haliaeetus albicilla) was virtually absent due to persecution and pollutants during the mid-20th century. The rapid growth of the eagle population from the 1980s onward initiated by extensive conservation efforts has not only brought the species back from the brink of extinction, but also caused growing predation pressure on its prey species, in particular the common eider (Somateria mollissima), which is the major prey of the eagles in the Åland islands and especially in the outer archipelago. In Lapland in northern Finland, where husbandry of semi-domestic reindeer is a traditional livelihood, concerns are rising that the expanding white-tailed eagle population poses a threat to reindeer calves. As top predators, the white-tailed eagles are sensitive to bioaccumulating hazardous substances. Despite the decreased levels of pollutants, the Baltic Sea is still the world’s most heavily polluted sea, while mercury levels in the major water bodies in Lapland, two artificial water reservoirs, are higher than in the Baltic. For successful conservation of both the white-tailed eagle and its prey species research is needed regarding the diet of the eagles and the mechanisms shaping the diet. This system also provides an opportunity to study the predator-prey dynamics following the rapid return of an apex predator to a system from where it has been virtually absent. In this thesis I cover (i) the prey use and nesting habitat choice of white-tailed eagles nesting in the Finnish coast and Lapland, (ii) the connections between the prey use and the nesting habitat, (iii) the use of reindeer calves as prey, (iv) the association between nesting white-tailed eagles and the spatiotemporal population trends of the common eider, and (v) the consequences of prey use and nesting site choice on the mercury burden in white-tailed eagle nestlings in Lapland. I found that the prey use of white-tailed eagles changed in time in the archipelago, and that it both in the archipelago and in the inland was influenced by the habitat in the nesting territories, which reflects the occurrence of prey species. In the inland, the white-tailed eagles preferred territories with higher proportions of lakes, peatbogs, and marshlands, which coincides with the higher occurrence of their preferred food source, fish. In the archipelago the main prey of the white-tailed eagles was common eider, which population in the Baltic has declined rapidly since a peak in 1997. The spatiotemporal changes in the core of the eider population distribution were influenced by the proximity of nesting white-tailed eagles. The eiders declined most in the outer archipelago and on unforested islands in the proximity of eagle nest. On the contrary, the population increased in the inner archipelago in areas with eagle nests. Finally, the prey use and nesting habitats influenced the eagles themselves. Elevated mercury burdens in white-tailed eagle nestlings in Lapland were linked with a diet on high trophic-level species and especially pike, the most important prey species in the area, as well as the proximity to a point source; the artificial reservoir of Porttipahta. As flexible opportunists, the white-tailed eagles should not be food-deprived even though some prey species would decline. Likewise, the prey species should not be over-exploited, as the eagles use alternative prey species when a species decline. Population-level eagle-induced shifts has moved the core of the eider population towards safer nesting environments in the inner archipelago. However, the very rapid decrease of eiders calls for close monitoring and conservation efforts of the species. As top predators, the white-tailed eagles are prone to accumulation of pollutants and are as such excellent sentinel species for environmental pollution. However, consequently they are also vulnerable and thus, even though the population today is viable, a continuum of the thorough monitoring of the white-tailed eagles is important. The ecosystem resilience is today severely challenged by anthropogenic impacts. Returning apex predators can improve the states of the ecosystems by e.g. preventing over-grazing, controlling the growth of prey populations and restricting invasive mesopredators. Successful co-existence with humans requires a general acceptance of the predators which only can be gained through cooperation and involvement of stakeholders and inhabitants that are affected by the matter.
... Samples of seven Baltic Sea species of different TLs were used. The species were chosen based on their ecological relevance for the Baltic region, established trophic relationships, and availability in the Swedish Environmental Specimen Bank (ESB), with an emphasis on species that have documented contaminant-related health effects (Bignert and Helander, 2015;de Wit et al., 2020;Möllmann et al., 2005;Rajasilta et al., 2019;Roos et al., 2012;Schiedek et al., 2006;Sonne et al., 2020). The investigated species could be divided into top consumers (four species), low-level consumers (two fish species) and filter feeders (one species). ...
Article
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High-resolution mass spectrometry (HRMS) based non-target screening (NTS) is a powerful approach for the simultaneous determination of multiple environmental contaminant classes in complex biota samples. In this study, trophic biomagnification factor (TMF) directed NTS was performed to find and (tentatively) identify known, emerging, and new chemical contaminants that are persistent and biomagnify in Baltic Sea biota. The investigated food web included seven species: one filter feeder (blue mussel, Mytilus edulis), two fish (eelpout, Zoarces viviparous; herring, Clupea harengus), two marine mammals (harbor porpoise, Phocoena phocoena; grey seal, Halichoerus grypus) and two birds (guillemot, Uria aalge; white-tailed sea eagle, Haliaeetus albicilla). The NTS procedure included extraction with organic solvent mixtures, two-step high-resolution gel permeation chromatography clean-up, Florisil® fractionation, gas chromatography (GC) HRMS analysis in electron ionization (EI) and electron capture negative ion chemical ionization (ECNI) modes, and NTS data processing. The latter was performed differently for the EI and ECNI data: the EI data were treated using a flexible and highly automated TMF-directed NTS workflow, whereas the ECNI data were treated with a simpler and less automated workflow that specifically screened for brominated compounds. The two workflows collectively revealed biomagnification (statistically significant TMF values) of >250 tentatively identified compounds, including legacy persistent organic pollutants (POPs), such as PCBs and PCB-related compounds, DDT and its metabolites, and organochlorine pesticides (OCPs), contaminants of emerging concern (CECs), and halogenated natural products (HNPs). Among the tentatively identified CECs, nine have not previously been reported in environmental biota samples. These included four polymer additives (used as antioxidants, rubber additives or plasticizers) and two cosmetic product additives (ethyl myristate and isopropyl palmitate). The CECs should be prioritized for future structure verification and quantification using reference standards.
... In the studied population, levels of legacy POPs measured in eggs and feathers from adult WTEs have been steadily decreasing over the 20 years prior to our study period (Helander et al., 2008;Sun et al., 2020), leading to improved breeding success since the 1980s (Helander et al., 2002). In the current study, sampling started in 1995 when DDE and PCB levels were below the thresholds for effects on reproduction (Bignert and Helander, 2015), which could explain the lack of relationships between telomere length and POP concentrations in our study. ...
Article
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Telomeres are used as biomarkers of vertebrate health because of the link between their length, lifespan, and survival. Exposure to environmental stressors appears to alter telomere dynamics, but little is known about telomere length and persistent organic pollutant (POP) exposure in wildlife. The white-tailed eagle (WTE; Haliaeetus albicilla) is an avian top predator that accumulates high levels of POPs and may subsequently suffer adverse health effects. Here we study the Baltic WTE population that is well documented to have been exposed to large contaminant burdens, thereby making it a promising candidate species for analyzing pollutant-mediated effects on telomeres. We investigated telomere lengths in WTE nestlings (n = 168) over 19 years and examined legacy POP concentrations (organochlorines and polybrominated diphenyl ethers) in whole blood and serum as potential drivers of differences in telomere length. Although we detected significant year-to-year variations in telomere lengths among the WTE nestlings, telomere lengths did not correlate with any of the investigated POP concentrations of several classes. Given that telomere lengths did not associate with POP contamination in the Baltic WTE nestlings, we propose that other environmental and biological factors, which likely fluctuate on a year-to-year basis, could be more important drivers of telomere lengths in this population.
... The degree to which a chemical bioaccumulates also influences the outcomes of chemical exposure and risk assessments (Swackhammer et al., 2009). Hazardous substances have accumulated at high levels in top predators in the Baltic Sea and previously caused reproductive failure and contributed to near extinction of grey seals (Halichoerus grypus) and white-tailed sea eagles (Haliaeetus albicilla; Roos et al., 2012;Bignert and Helander, 2015). Since the 1970s-1980s, concentrations of several contaminants in biota have declined significantly due to strict regulations (Nyberg et al., 2015), allowing for top predator populations to recover (Helander et al., 2008;Roos et al., 2012;Reusch et al., 2018). ...
Article
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Food webs are central entities mediating processes and external pressures in marine ecosystems. They are essential to understand and predict ecosystem dynamics and provision of ecosystem services. Paradoxically, utilization of food web knowledge in marine environmental conservation and resource management is limited. To better understand the use of knowledge and barriers to incorporation in management, we assess its application related to the management of eutrophication, chemical contamination, fish stocks, and non-indigenous species. We focus on the Baltic, a severely impacted, but also intensely studied and actively managed semi-enclosed sea. Our assessment shows food web processes playing a central role in all four areas, but application varies strongly, from formalized integration in management decisions, to support in selecting indicators and setting threshold values, to informal knowledge explaining ecosystem dynamics and management performance. Barriers for integration are complexity of involved ecological processes and that management frameworks are not designed to handle such information. We provide a categorization of the multi-faceted uses of food web knowledge and benefits of future incorporation in management, especially moving towards ecosystem-based approaches as guiding principle in present marine policies and directives. We close with perspectives on research needs to support this move considering global and regional change.
... Bignert et al. (1995) showed that replacement eggs had significantly higher levels of DDT and PCBs than first-laid eggs. Guillemots can regulate their reproductive effort by varying egg size or the amount of resources allocated to the egg (Birkhead and Harris, 1985), and guillemots may use more stored reserves from body fat to form the replacement egg as significant energy has already been expended forming the first-laid egg (Bignert and Helander, 2015). However, despite being replacement eggs, guillemot eggs from Aughris Head in this study had significantly lower levels of Σ16PCBs, Σ6PBDE, HCB and ΣDDT than all other sites. ...
Article
Guillemot eggs from multiple Irish colonies and one Welsh colony were analysed for legacy pollutants such as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and other organochlorine compounds (OCs), as well as metals. Stable isotope ratios of carbon (δ¹³C) and nitrogen (δ¹⁵N) were measured in eggs to understand the influence of diet on contaminant levels detected. Wide-scope target and suspect screening techniques were used on a single guillemot egg, providing novel information on contaminants of emerging concern. Stable isotope ratio analysis showed that guillemots from Great Saltee Island and Lambay Island (Ireland’s east coast) had a similar carbon source (δ¹³C) and fed at similar trophic levels (δ¹⁵N), pollutant levels were higher in eggs from Lambay Island near Dublin, Ireland’s industrialised capital city. Guillemot eggs from Aughris Head (Atlantic west coast of Ireland), and Skomer Island (Wales) had differing isotopic niches to other colonies. Egg samples from Aughris Head had the lowest levels of pollutants in this study (with the exception of mercury) and amongst the lowest levels reported worldwide. In contrast, Skomer Island had the highest level of pollutants with higher concentrations of Σ16PCB, Σ6PBDE and HCB than Irish colonies, most likely a result of its proximity to historically industrial areas. Levels of PCBs, p,p’ –DDE and mercury in guillemot eggs have decreased over time according to this study, in concurrence with worldwide trends. Levels of pollutants in guillemot eggs, in this study, fall below existing thresholds for adverse effects in other species, with the exception of mercury.
... International restrictions introduced in the 1970s and 1980s [3,4] reduced levels of certain AHSs in the environment, and many affected populations recovered. However, the levels of legacy AHSs in the Baltic Sea region have stopped declining rapidly in recent years [3,[6][7][8][9]. Furthermore, new industrial chemicals that may potentially be of concern are produced every year [3,4,10]. ...
Article
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The health of key species in the Baltic region has been impaired by exposure to anthropogenic hazardous substances (AHSs), which accumulate in organisms and are transferred through food chains. There is, thus, a need for comprehensive characterization of the occurrence and accumulation of AHSs in the ecosystem. In this study, we use a non-target screening (NTS) approach for this purpose. A major challenge in NTS of biological samples is the removal of matrix components such as lipids that may interfere with the detection and identification of compounds of interest. Here, we combine gel permeation chromatography with Florisil® column fractionation to achieve sufficient lipid removal for gas chromatography–high-resolution mass spectrometry analysis using electron ionization (EI) and electron capture negative ion chemical ionization (ECNI). In addition, we present new data processing workflows designed to systematically find and identify frequently occurring and biomagnifying AHSs, including known, emerging, and new contaminants. Using these workflows, we discovered a wide range of contaminants in tissue samples from blue mussels, fish, and marine mammals, and calculated their biomagnification factors (BMFs). Compounds with BMFs above 1 for herring and at least one marine mammal included legacy chlorinated pollutants (polychlorinated biphenyls, DDTs, chloro-benzenes/cyclohexanes, chlordanes, toxaphenes, dieldrin), polybrominated diphenyl ethers (PBDEs), and brominated biphenyls. However, there were also several halogenated natural products (halogenated methoxylated brominated diphenyl ethers, 1′-methyl-1,2′-bipyrroles, 1,1′-dimethyl-2,2′-bipyrroles, and the halogenated monoterpene mixed halogenated compound 1) as well as the novel flame retardant Dechlorane 602 and several polycyclic aromatic hydrocarbons, terpenoids, and steroids. The legacy pollutants exhibited the expected biomagnification behavior, demonstrating the utility of the unguided data processing workflow.
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Knowledge base for ecosystem-based marine management in the Bothnian Sea (Swedish Language).
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Struwe-Juhl, B. & R. Schmidt (2002): Möglichkeiten und Grenzen der Individualerkennung von Seeadlern (Haliaeetus albicilla) anhand von Mauserfederfunden in Schleswig-Holstein (1955-2000). Corax 19, Sonderheft 1: 37-50. Zwischen 1955 und 2000 wurden in den Seeadlerrevieren von Schleswig-Holstein systematisch Mauserfedern gesammelt und hinsichtlich der individuellen Paarzusammensetzung analysiert (581 Schwanzfedern und 382 Handschwingen aus maximal 22 Brutrevieren in 1999). Die Individualer-kennung erfolgt anhand der Variabilität von Federmerkmalen, wobei das Pigmentmuster der Schwanzfedern und die Länge der Schwung-und Steuerfedern die Hauptmerkmale für die Unter-scheidung der Individuen sind. Adulte Seeadler erlangen die spezifische Pigmentierung ihrer Schwanzfedern ab dem 5. Kalender-jahr (Kj.), und die Federlänge ist ab dem 7. Kj. weitgehend konstant. Ab diesem Alter variieren die-se Federmerkmale nur noch geringfügig, so dass sie in geografisch begrenzten Populationen zur in-dividuellen Erkennung genutzt werden können. Eine Einschränkung der Mauserfederanalyse er-gibt sich unter Umständen daraus, dass sich die Pigmentmuster verwandter Seeadler(weibchen) sehr ähnlich sehen können, wodurch die Aussagekraft dieses Merkmals eingeschränkt wird. Seeadlerweibchen sind in der Regel größer als die Männchen. Dieser Geschlechtsdimorphismus findet sich auch in der Morphologie der Großfedern wieder.
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DDE residues in kestrel eggs collected from the Ithaca, New York area averaged 35, 42, 33 and 37 ppm for the years 1969, 1970, 1971 and 1972, respectively. Based on Ratcliffe's Index, eggshells of the local population averaged 10% thinner than pre DDT eggshells. A dose response relationship is established for dietary DDE and eggshell thinning in a captive kestrel population. Statistical analysis revealed that the correlative relationship between DDE in the egg and eggshell thinning is the same for both captive experimental birds and the wild population. A discussion of organochlorines, eggshell thinning and the decline of several populations of North American raptors concludes that a causal relationship exists between the ingestion of prey highly contaminated with DDE and the consequent eggshell thinning and eggshell breakage. The breeding failure that follows and subsequent population declines of several raptor populations proceeds in a straightforward, logical and well documented sequence.
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Bycatch of common guillemots (Uria aalge) appears to be the single most serious threat to the population, and the proportion of recoveries of ringed birds in fishing gear, compared with other finding circumstances, has significantly increased during a 28 year period (P<0.01). Out of 1952 ringed common guillemots reported found between 1972 and 1999 in the Baltic Sea, 980 (50.2%) were caught in fishing gear. The bycatch in set gillnets for cod (Gadus morhua) constituted 22.3%, drift gillnets for salmon (Salmo salar) 65.5%, and other fishing gear 12.2%. The proportion of recoveries in cod gillnets has significantly increased during the study gillnets. The Swedish fishing effort. follows period (P < 0.05), while no clear trend was observed in the recoveries in salmon a similar pattern for cod but has decreased for salmon. The observed increased use of cod gillnets in the Baltic Sea may have contributed to the observed decrease in adult survival rate, and we provide two different estimates suggesting that significant proportions of the guillemot population are caught annually in the Baltic Sea gillnet fishery. We suggest several available techniques to reduce bycatch in the Baltic Sea fishery.
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"An important, controversial account ... of the way in which man's use of poisons to control insect pests and unwanted vegetation is changing the balance of nature." Booklist.
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Within Europe, the Marine Strategy Framework Directive (MSFD) is aimed at addressing the chemical status and quality of the marine environment. One of the main goals is to achieve Good Environmental Status (GES) in the marine environment. Environmental monitoring of biota e.g., Baltic herring and guillemot eggs, is conducted annually in Sweden to follow temporal changes in environmental contaminants. To determine the suitability of guillemot eggs as a sentinel species for investigating GES, we compared temporal trends of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) and dioxin-like polychlorinated biphenyls (dl-PCBs) in these two species from single sampling sites within Sweden. Lipid content from guillemot eggs was consistently high and stable (yearly mean for > 40 years, ∼12%) compared to that of herring (yearly mean for > 20 years, ∼3%). A significant decreasing trend of ΣPCDD/F in TEQ WHO1998 was observed in guillemot eggs, but no trend was seen in herring. CB118 significantly decreased in both species, but in the last 10 years this decrease was not significant in herring. A number of advantages, such as high lipid content in the egg and a low coefficient of variation make guillemot suitable as a sentinel species. The advantages and disadvantages of using either guillemot eggs or Baltic herring are compared.
Article
Literature has been reviewed concerning shell thinning in avian eggs by environmental pollutants. Field evidence indicates that the declines in shell thickness observed in certain species in North America and Great Britain since the Second World War have been largely caused by residues of pp′-DDE or other compounds or metabolites of the DDT group. In North America, polychlorinated biphenyls and cyclodiene insecticides have played no more than minor roles, although in Britain cyclodienes have probably made a significant contribution. Mercury compounds are not apparently associated with the shell thickness declines.Results from controlled experiments, in which laying birds have been exposed to pollutants, generally support these suggestions. Laboratory investigations indicate an interspecific difference in shell thinning response, gallinaceous species tending to be the most resistant and falcons the most susceptible.In a laying bird, organochlorine residues affect many biochemical mechanisms known to be essential for proper shell formation and the extent of the contribution of each affected mechanism towards decreasing shell thickness probably depends on variables such as species and environmental conditions. There is no evidence to suggest that one mechanism is always dominant irrespective of the conditions.In North America shell thinning has often been associated with population decreases, but in Britain declines in shell thickness are not thought to be responsible for the population decreases observed in certain raptor species.