Björn Helander

The Role of DDE, PCB, Coplanar PCB and Eggshell Parameters for Reproduction in the White-tailed Sea Eagle (Haliaeetus albicilla) in Sweden

Abstract The reproduction of white-tailed sea eagles was monitored in 1964–1999 in 3 differently contaminated sub-populations: Baltic Sea coast (Bp), inland central Sweden (Ip) and Lapland (Lp). 249 dead eggs from 205 clutches were obtained for analyses of DDE and PCBs and for eggshell measurements. A desiccation index (Di) value was calculated for each egg as a measure of water loss through the shell. In the highly contaminated Bp, p,p´-DDE concentrations in the eggs decreased continuously and 5-fold during the study period and PCB concentrations decreased 3-fold from the mid 1980s. The PCB pattern changed slightly over time towards more high-chlorinated congeners but the relative toxicity of the PCB mixture, expressed as 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TEQ), remained constant and TEQ can be assumed to have decreased in a similar way as PCB over time. Productivity (P), shell thickness (St), shell index (Si) and Di increased over time in the Bp but no change in Di or productivity occurred in the Lp, where residue concentrations were 5–8 times lower. P of the Bp was not correlated to St or Si but was negatively correlated to Di, DDE and PCB. An S-shaped dose-response relationship was indicated between P and DDE. After 1988, when the PCB/DDE ratio was considerably higher than previously, PCB but not DDE concentrations were significantly higher in eggs with dead embryos as compared to undeveloped eggs, implying lethal concentrations of PCB, and a LOEL of 320 pg g−1 TEQ is suggested for embryo mortality. In a subset of 21 eggs, representing productive and unproductive females, analyzed for a selection of coplanar PCB congeners, tris(4-chlorophenyl) methanol and bis(4-chlorophenyl) sulphone, there was no evidence for a correlation between P and any of these compounds. A reduction in residue concentrations in old females did not lead to increased P or improved Di-values, indicating a remaining effect from a previous, higher exposure to contaminants. The inability to reproduce included a high rate of undeveloped eggs, indicating effects at a prezygotic stage. P showed the strongest correlation with Di, and Di was most strongly correlated to DDE. Thus, the remaining effect of previous exposure resulted in a stronger correlation to the symptom (Di) rather than to the suggested causative agent (DDE). LOEL values for depressed P were estimated at 120 µg g−1 DDE and 500 µg g−1 PCB (lipid basis). It is concluded that the major reason for depressed P during the study period was DDE, but that effects also from PCB were largely concealed by the effects from DDE.

Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline

Most of the white-tailed eagle (Haliaeetus albicilla) populations in Europe experienced dramatic declines during the twentieth century. However, owing to intense conservation actions and the ban of DDT and other persistent pollutants, populations are currently recovering. We show that despite passing through demographic bottlenecks, white-tailed eagle populations have retained significant levels of genetic diversity. Both genetic and ringing data indicate that migration between populations has not been a major factor for the maintenance of genetic variability. We argue that the long generation time of eagles has acted as an intrinsic buffer against loss of genetic diversity, leading to a shorter effective time of the experienced bottleneck. Notably, conservation actions taken in several small sub-populations have ensured the preservation of a larger proportion of the total genetic diversity than if conservation had focused on the population stronghold in Norway. For conservation programmes targeting other endangered, long-lived species, our results highlight the possibility for local retention of high genetic diversity in isolated remnant populations.

Using Raptors as Environmental Sentinels: Monitoring the White-tailed Sea Eagle Haliaeetus albicilla in Sweden

Abstract This paper summarizes results from the monitoring of reproduction of white-tailed sea eagle in Sweden 1965–2006. Since 1989 the eagle population on the Swedish Baltic coast has been included in the National Environment Monitoring Program as an indicator species for potentially harmful chemicals. The percentage of successfully reproducing pairs and nestling brood size decreased in synchrony with rising concentrations of contaminants in the 1950s on into the 1970s. Mean productivity was 1.3 young per pair prior to 1950 and decreased to 0.3 in 1965–1985. Dichlorodiphenyldichloroethene (DDE) in eagle eggs decreased from a range of annual means in 1965–1974 of 600-1200 μg g−1 (lipid weight) to 60–140 μg g−1 in 1996–2005. Total polychlorinated biphenyl (PCB) concentrations averaged above 1000 μg g−1 into the early 1980s and remained in the range of 250–500 μg g−1 in 1996–2005. Productivity began to improve when concentrations of DDE and PCBs dropped below approximately 300 and 800 μg g−1, respectively. Brood size remains below the pre-1950 level in one coastal region, indicating a possible impact from other contaminants. The power to detect significant trends under the program is presented and discussed: if white-tailed sea eagle reproduction had been monitored earlier during the 20th century, the negative impact of dichlorodiphenyltrichloroethane (DDT, source of DDE) would have been signaled as early as the 1950s in the Baltic Sea. The dramatic fall of white-tailed sea eagle reproduction under the influence of DDT and PCBs, and the subsequent rise following their ban, illustrates the usefulness of raptors like sea eagles as sentinels for environmental pollutants.

Status of Baltic grey seals: Population assessment and extinction risk

The grey seal ( Halichoerus grypus ) population in the Baltic Sea is recovering after a century of bounty hunting and 3 decades of low fertility rates caused by environmental pollution. A conservative estimate of the population size in 2003 was 19,400 animals, and available data suggest an annual rate of increase of 7.5% since 1990. The growing population has led to increased interactions with the fishery, and demands are being raised for the re-introduction of the hunt. We provide a demographic analysis and a risk assessment of the population, and make recommendations on how to decrease the risk of over exploitation. Although hunting increases the risk of quasi-extinction, the risk can be significantly reduced by the choice of a cautious hunting regime. The least hazardous regimes allow no hunting below a ‘security level’ in population size. Obviously, to implement such a hunting regime detailed knowledge of the population size and growth rate is required. It is not possible to estimate “true” risks for quasi-extinction, but we used an approach where the relative difference for different scenarios can be compared. With a security level at 5,000 females, the population quasi-extinction risk increases 50 fold at an annual hunt of 500 females compared with a scenario with no hunting. The risk of quasi-extinction is very sensitive to declines in the mean growth rate and to increased variance in growth rate. The variance in the population estimates over the last 14 years imply that it would take 9 years to detect a decline from 1.075 to 1.027 in the rate of population increase. We also show how the age composition of killed animals influences the impact of the hunt. The overall recommendation is that hunting should be kept to a minimum, carefully documented and accompanied by close population monitoring.

Photo-identification, Site Fidelity, and Movement of Female Gray Seals (Halichoerus grypus) Between Haul-outs in the Baltic Sea

Abstract The growing gray seal population in the Baltic Sea has led to increased conflicts with fisheries. Despite limited data on gray seal ecology, management measures, such as culling, have been implemented recently. We studied movements and site fidelity of Baltic gray seals using mark-recapture analysis based on photographic identification of individuals (photo-id). Seals were photographed at the major summer haul-out sites. Profile photographs of the head and neck were matched using purpose-written software to generate a database of capture histories from 1995–2000. The haul-outs were grouped into seven areas. Darrochs method (20) for a two-sample capture-recapture census was adapted to estimate rates of movement between the areas. The majority of seals were estimated to remain within the same area, suggesting that Baltic gray seals exhibit a high degree of site fidelity during the summer, and that fidelity to a site lasts for more than one season.

Ingestion of lead from ammunition and lead concentrations in white-tailed sea eagles (Haliaeetus albicilla) in Sweden.

In this study we show for the first time that lead poisoning from ammunition is a significant mortality factor for white-tailed sea eagle (WSE) (Haliaeetus albicilla) in Sweden. We analyzed 118 WSEs collected between 1981 and 2004 from which both liver and kidney samples could be taken. A total of 22% of all eagles examined had elevated (>6 microg/gd.w.) lead concentrations, indicating exposure to leaded ammunition, and 14% of the individuals had either liver or kidney lead concentrations diagnostic of lethal lead poisoning (>20 microg/gd.w.). Lead concentrations in liver and kidney were significantly correlated. In individuals with lead levels <6 microg/g, concentrations were significantly higher in kidney than in liver; in individuals with lead levels >20 microg/g, concentrations were significantly higher in liver. The lead isotope ratios indicate that the source of lead in individuals with lethal concentrations is different from that of individuals exhibiting background concentrations of lead (<6 microg/gd.w.) There were no significant sex or age differences in lead concentrations. A study from the Baltic reported in principle no biomagnification of lead, but background lead concentrations in WSE liver in this study were still four to >10 times higher than concentrations reported for Baltic fish from the same time period. In contrast to other biota there was no decrease in lead concentrations in WSE over the study period. The proportion of lead poisoned WSE remained unchanged over the study period, including two years after a partial ban of lead shot was enforced in 2002 for shallow wetlands. The use of lead in ammunition poses a threat to all raptors potentially feeding on shot game or offal. The removal of offal from shot game and alternatives to leaded ammunition needs to be implemented in order to prevent mortality from lead in raptors and scavengers.

Improved reproductive success in otters (Lutra lutra), grey seals (Halichoerus grypus) and sea eagles (Haliaeetus albicilla) from Sweden in relation to concentrations of organochlorine contaminants

We studied indices of reproductive outcome in three aquatic species in relation to organochlorine concentrations during four decades. In female otters, the frequency of signs of reproduction increased after 1990. In grey seals, pregnancy rate increased 1990-2010 and uterine obstructions ceased after 1993. The frequency of uterine tumours was highest 1980-2000. The number of sea eagle nestlings per checked nest increased 1985-2000, while the frequency of desiccated eggs decreased. Organochlorine concentrations decreased at annual rates between 3.5 and 10.2%. The estimated mean concentration (mg/kg lw) for total-PCB decreased from 70 to 8 (otters), from 110 to 15 (seals) and from 955 to 275 (eagles). The corresponding concentrations for ΣDDT decreased from 3.4 to 0.2 (otters), from 192 to 2.8 (seals) and from 865 to 65 (eagles). This study adds evidence to support the hypothesis that PCBs and DDTs have had strong negative effects on the reproduction and population levels of these species.

Morphological and genetic sex identification of white-tailed eagle Haliaeetus albicilla nestlings

Identifying the sex of bird nestlings is relevant to studies of behaviour and ecology and is often a central issue in the management of endangered or captive populations. The white-tailed eagle Haliaeetus albicilla is a formerly threatened Eurasian raptor which is closely monitored in many countries due to its high exposure to environmental pollutants in the food chain. The aim of this study was to evaluate the reliability of sex identification methods for white-tailed eagle nestlings based on morphological measurements that can be recorded at the nest by a single person and with minimum disturbance. The sex of each bird was independently determined using molecular (genetic) methods. One measure of tarsus width allowed the correct identification of sex for 96% of the nestlings from southern and central Sweden. However, we found that the criteria for sex identification were not directly applicable to the population in Swedish Lapland, where nestlings are typically thinner, probably due to a limited food supply. These results show that sexing in the field of white-tailed eagle nestlings can be feasible with high accuracy based on a limited number of measurements. However, the criteria employed to separate sexes may have to be adjusted for each population.

Sublethal Lead Exposure Alters Movement Behavior in Free-Ranging Golden Eagles

Lead poisoning of animals due to ingestion of fragments from lead-based ammunition in carcasses and offal of shot wildlife is acknowledged globally and raises great concerns about potential behavioral effects leading to increased mortality risks. Lead levels in blood were correlated with progress of the moose hunting season. Based on analyses of tracking data, we found that even sublethal lead concentrations in blood (25 ppb, wet weight), can likely negatively affect movement behavior (flight height and movement rate) of free-ranging scavenging Golden Eagles (Aquila chrysaetos). Lead levels in liver of recovered post-mortem analyzed eagles suggested that sublethal exposure increases the risk of mortality in eagles. Such adverse effects on animals are probably common worldwide and across species, where game hunting with lead-based ammunition is widespread. Our study highlights lead exposure as a considerably more serious threat to wildlife conservation than previously realized and suggests implementation of bans of lead ammunition for hunting.

Polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans and non-ortho-PCBs in eggs of white-tailed sea eagles collected along the Swedish coast in the Baltic Sea.

Concentrations of polychlorinated dibenzo-p-dioxins (PCDD), polychlorinated dibenzofurans (PCDF), and dioxin-like non-ortho-PCBs were measured in white-tailed sea eagle (WTSE) eagle eggs collected along the Swedish coast of the Baltic Sea during the period 1992-2004. The eggs represent two different subpopulations with significantly different nestling brood sizes; the Baltic Proper (BP) with an approximately normal nestling brood size (1.62), and the south Bothnian Sea (sBS) with reduced nestling brood size (1.22) combined with a significantly higher rate of dead eggs. The aim was to investigate if this difference in reproductive outcome was linked to differences in exposure to dioxin-like compounds. Three eggs collected in Greenland in 2000 were included in the study to provide a reference sea eagle population outside of the Baltic Sea region. The concentrations of ∑PCDD, ∑PCDF and ∑non-ortho-PCB in the two subpopulations from the Baltic Sea (BS) region ranged from 0.41-4.1, 1.2-5.3 and 180-970 ng/g lipids, respectively, while in the Greenland population the ranges were 0.11-0.16, 0.22-0.33 and 57-83 ng/g lipid, respectively. 2,3,4,7,8-PCDF was the predominant congener in all areas and accounted for on average 31-49% of the total ∑PCDD/F concentrations. The total toxic equivalents (TEQ) in sBS WTSEs were higher (approximately 39 ng TEQ/g lipid) than reported in eggs for many other birds, and the major contributors to the TEQ in the Baltic Sea were the non-ortho-PCBs. A principal component analysis (PCA) showed a difference in congener pattern between the two Baltic regions that was statistically significant (Hotellings T(2) test). We found no significant differences in the total TEQ between the two populations (sBS-BP) and thus no evidence was found linking the reproductive impairment in WTSE in sBS to the concentrations of PCDD/Fs or non-ortho-PCBs in the eggs.