The status of the Baltic Sea marine environment in terms of contamination by hazardous substances is assessed using several core indicators. Each indicator focuses on one important aspect of the complex issue. In addition to providing an indicator-based evaluation of the status of white-tailed sea eagle productivity, this indicator also contributes to the overall hazardous substances assessment, along with the other hazardous substances core indicators.
The white-tailed sea eagle populations declined significantly were even exterminated in many European countries in the early 1900s due to strong persecution in the 19th and early 20th centuries. The population increased again due to protection measures. A second decline began in the 1950s and continued into the 1960s and 1970s due to organic pollutants, mainly DDE (a metabolite of DDT) which caused structural changes and thinning of egg shells, and PCB which caused embryo mortality, and hence, wide-spread failure in reproduction. Reproduction in the Baltic Sea eagle population in the 1970s was reduced to one fifth of the pre-1950 background level. Following bans of DDT and PCB during the 1970s, the Baltic white-tailed sea eagle productivity began to recover from the mid-1980s, and since the mid-1990s is largely back to pre-1950 levels. The population on the Swedish Baltic coast has increased at 7.8% per year since 1990.
The improvement in reproduction of the Baltic white-tailed sea eagle populations came no earlier than 10 years after most countries around the Baltic had implemented bans of DDT and PCB. This is a clear reminder of the potentially long-term effects of persistent pollutants. The subsequent recovery is nevertheless important evidence of successful results due to wise political decisions.
The indicator on white-tailed sea eagle productivity addresses the Baltic Sea Action Plan (BSAP) Biodiversity and nature conservation segment's ecological objective 'Viable populations of species'.
The core indicator also addresses the following qualitative descriptors of the MSFD for determining good environmental status (European Commission 2008):
Descriptor 1: 'Biological diversity is maintained. The quality and occurrence of habitats and the distribution and abundance of species are in line with prevailing physiographic, geographic and climatic conditions';
Descriptor 4: 'All elements of the marine food webs, to the extent that they are known, occur at normal abundance and diversity and levels capable of ensuring the long-term abundance of the species and the retention of their full reproductive capacity'.
Descriptor 8: 'Concentrations of contaminants are at levels not giving rise to pollution effects'.
and the following criteria of the Commission Decision (European Commission 2010):
As a top predator in aquatic ecosystems in general, the white-tailed sea eagle is relevant for the Water Framework Directive (2000/60/EC) in relation to the objective Chemical quality, as indicator for detrimental effects of pollutants.
The EU Birds Directive (79/409/EEC) lists the white-tailed sea eagle in Annex I, binding member states to undertake measures to secure reproduction and survival of the species. The species is also listed in the following international conventions:
Monitoring of sea eagle population health as an environmental indicator, as well as monitoring of contaminants in eagles and their prey, is recommended in an international Species Action Plan adopted under the Bern Convention in 2002. In Sweden, reproductive parameters of white-tailed sea eagle are included in the national environment monitoring program as indicators for harmful effects of contaminants since 1989. White-tailed sea eagle productivity, and eggshell thickness of white-tailed sea eagle and guillemot, is used in the Swedish implementation of the MSFD as indicators for effects from harmful substances (HVMFS 2012:18, 8.2.A and 8.2.B).
The white-tailed sea eagle is the ultimate top predator of the Baltic ecosystem, feeding on fish, sea birds, and seals, and is thus strongly exposed to persistent chemicals that magnify in the food web. It was the first species that indicated deleterious effects from environmental pollutants in the Baltic Sea.
Within the Helsinki Convention area, white-tailed sea eagle preys primarily on waterfowl and fish, and to some extent on mammals, largely as carrion (seals) (Relevance table 1). The white-tailed sea eagle is an opportunistic hunter and the food it consumes largely reflects the availability of potential prey. Fish that dwell in shallow waters or close to the surface are particularly vulnerable to predation. Common fish prey species in the Baltic Sea coastal ecosystems include pike (Esox lucius), bream (Abramis brama), Ide (Leuciscus idus) and perch (Perca fluviatilis). A species that has increased strongly as prey in recent years in the Baltic Proper is garfish (Belone belone), probably as a result of increased availability but possibly also as a substitute for local decreases in the abundance of pike. Most common among bird prey are eider (Somateria mollissima), mergansers (Mergus merganser, M.serrator), mallard (Anas platyrhynchos), cormorants (Phalacrocorax carbosinesis), gulls (Laridae spp.), great-crested grebe (Podiceps cristatus), and coot (Fulica atra). A clear shift from a dominance of fish prey near the mainland shore to a dominance of bird prey in the outer archipelago has been observed (Helander 1983). A shift among bird species has also been observed, reflecting differences in availability from mainland to outer coast areas. A decrease in the abundance (and thus availability) of eider has been compensated for by the increase in abundance of cormorants. The prey distributions seem to be largely similar in different parts of the Baltic Sea, but the proportions of the prey species have not been studied in all sub-basins.
Relevance table 1. Prey of white-tailed sea eagle in the Baltic Sea sub-basins.
In addition to being a top predator, the white-tailed sea eagle has other features that are favourable from a monitoring perspective. Territorial adults on the Baltic Sea coast are mainly sedentary and thus reflect the regional contaminant situation. Mating pairs generally pair for life and remain at the same breeding site, with sites commonly used over many generations of eagles. This provides very good opportunities for long-term monitoring and detailed studies. A large portion of breeders in the Baltic Sea region are currently ringed, improving possibilities for study of individual birds over time.
Contamination by hazardous substances
Enhanced mortality from collisions (trains, wind farms etc.).
Enhanced mortality from secondary poisoning by lead ammunition.
Vulnerable to direct persecution (now illegal).
Habitat loss and prey depletion are potentially serious future threats.
The productivity of the white-tailed sea eagle is affected by several human pressures that affect the nestling brood size (number of nestlings) and breeding success (success in raising at least one nestling per pair).
Relevance figure 1. Relationship of white-tailed sea eagle productivity parameters and underlying pressures. "Nest losses (weak trees)" within "Human induced breeding failures" refers to an increasing shortage of suitable nest trees in cultivated forests.
The human pressure that has most clearly affected white-tailed sea eagles after the species was legally protected is the introduction of hazardous substances to the environment. Chemical analyses of the contents of collected dead eggs have provided possibilities to study relationships between the concentrations of contaminants and reproduction. Tissue and egg samples of white-tailed sea eagles have contained among the highest residue concentrations of persistent organochlorine contaminants (e.g. DDTs and PCBs) and heavy metals ever documented in the Baltic Sea area, and worldwide (Henriksson et al. 1966; Jensen 1966; Jensen et al. 1972; Koivusaari et al. 1980; Helander 1994b; Helander et al. 1982, 2002, 2008; Olsson et al. 2000; Nordlöf et al. 2010). Furthermore, studies of individual eagles over time showed that females that were exposed to high concentrations of contaminants during the 1960s and 1970s remained unproductive after residue concentrations in their eggs had declined, indicating persistent effects from previous exposure (Helander et al. 2002).
Trends in productivity and residue concentrations of DDE and PCBs show that residue concentrations of DDE have now generally declined below an estimated critical threshold level for affecting reproduction (Relevance figure 2), but exceptions with very high concentrations have turned up during 2009-2013 among sea eagle eggs from the Gulf of Bothnia.
Relevance figure 2. Mean annual productivity (number of nestlings per checked occupied territory) and residue concentrations of DDE and total-PCB (µg/g, lipid weight) in white-tailed sea eagle eggs from the Swedish Baltic coast during 1965-2013. The shaded green area in the left graph indicates a range of concentrations below a previously estimated lowest-observable-effect-level (LOEL) for DDE according to Helander et al. (2002). Large dots = annual geometric means; small dots = individual clutches; vertical lines = 95% confidence limits (for sample sizes > 3). Regression lines for DDE and PCB in the eggs decreased significantly during the study periods (p<0.001). Productivity of the coastal population increased significantly (p<0.001). In a reference freshwater population in Swedish Lapland (not shown here), the concentrations of DDE were below the estimated LOEL and there was no statistically significant change in productivity over the study period.
Since predatory birds are highly exposed to persistent chemicals they are useful for detecting the presence of 'new' pollutants that are potentially harmful, as illustrated by the discovery of PCBs in 1966 in a Baltic white-tailed sea eagle (Jensen 1966) and the discovery of the flame retardant congener PBD-209 in peregrine falcon eggs in 2004 (Lindberg et al. 2004). Residue concentrations of brominated flame retardants have been investigated in eagle egg samples from Sweden, (Nordlöf et al. 2010) and concentrations in the Baltic samples were three and six times higher than those from inland samples from southern Sweden and Lapland, respectively. Lethal poisoning connected with consumption of lead ammunition has also been observed to be an important cause of death in white-tailed sea eagle populations (Krone et al 2006).
The massive development of wind power parks can lead to a significant increase in mortality among white-tailed sea eagles and can be seen as a reduction in breeding success and productivity (Dahl et al. 2012), but not in nestling brood size. Weather conditions can affect breeding success and productivity, and it will be interesting to follow the possible effects due to climate change.
In theory, also food shortages affect brood size and breeding success, but this has so far not been observed in the Baltic Sea population, where there has been, so far, plenty of food. Body mass can be indicative of food stress and health and such data can usually be easily obtained when assessing reproductive output in the nests and handling nestlings.
Using white-tailed sea eagle productivity as a core indicator for assessing status in relation to hazardous substances relies on the experience of the effects of exposure to persistent contaminants on this species over five decades on the Baltic Sea coast. If white-tailed sea eagle reproduction had been monitored in the Baltic Sea earlier during the 20th century, then the negative impact of DDT could have been noticed already in the 1950s. Retrospective studies have shown a significant drop in white-tailed sea eagle breeding success and nestling brood size already in the 1950s, with a further decrease during the 1960s and 1970s (Helander 1985). High concentrations of DDTs and PCBs in white-tailed sea eagle eggs were reported early from Finland (Koivusaari et al. 1980) and Sweden (Helander et al. 1982) and significant relationships were shown between productivity and residue concentrations of DDE and PCB in white-tailed sea eagle eggs (Helander et al. 1982, 1994b, 2002, 2008).
The productivity of white-tailed sea eagle in the coastal zone of different parts of the Baltic Sea is an indicator describing not only the effects from biomagnification of contaminants, but also persecution, disturbance of nest sites, food availability and availability of suitable nesting sites. Thus, it describes in reproductive terms the condition of the population and indirectly indicates the potential for increased abundance and distribution. This indicator combines the breeding success and brood size into a single indicator and assesses the reproductive output of the population. It is a useful indicator in studies on relationships between reproduction and human pressures and also a vital parameter in assessments of the state of populations from management perspectives.
Brood size is a precise parameter following the number of nestlings produced per nest containing young. This is a good indicator for impacts of hazardous substances because as top predators, white-tailed sea eagles accumulate persistent toxins which in turn can cause egg mortality. Breeding success (per cent pairs in the population that produce young) is another indicator for egg mortality, including effects from contaminants and also other anthropogenic disturbance as well as natural factors such as weather, and density dependent breeding failures.