High levels of perfluoroalkyl acids in eggs and embryo livers of great cormorant (Phalacrocorax carbo sinensis) and herring gull (Larus argentatus) from Lake Vänern, Sweden

In the eggs and developing chick livers in the two wild bird species, great cormorant and herring gull, the concentrations of a range of 15 perfluoroalkyl acids (PFAAs) were determined. Eggs of the two species were collected from Lake Vänern, Sweden, and analysed either as undeveloped egg (whole egg or separated into yolk and albumen) or incubated until start of the hatching process when the chick liver was removed and analysed. High levels of PFAAs were found in all matrixes except albumen. The predominant PFAA was perfluorooctane sulfonate (PFOS), which was found in the μg/g wet weight (ww) range in some samples of cormorant whole egg, yolk and liver and herring gull egg yolk and liver. The average concentration in yolk was 1,506 ng/g ww in cormorant and 589 ng/g ww in herring gull. The average liver concentrations of PFOS were 583 ng/g ww in cormorant and 508 ng/g ww in herring gull. At these concentrations, biochemical effects in the developing embryo or effects on embryo survival cannot be ruled out. For perfluoroalkyl carboxylates (PFCAs), the liver/egg and liver/yolk concentration ratios increased with PFCA chain length in cormorant but not in herring gull, indicating that chain length could possibly affect egg-to-liver transfer of PFCAs and that species differences may exist.     

Environmental pollutants in the Swedish marine ecosystem, with special emphasis on polybrominated diphenyl ethers (PBDE)

Levels of polybrominated diphenyl ethers (PBDEs), polybrominated biphenyls (PBBs), polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane (DDT) and perfluorinated organic compounds (PFCs) were analysed in whole herring (Clupea harengus) and sprat (Sprattus sprattus), eggs from common eider (Somateria mollissima) and eggs and livers from herring gull (Larus argentatus) from the Swedish west coast. The contaminant values obtained were compared with published values from the Arctic marine ecosystem. Tetra- and penta-brominated PBDEs were detected at low levels in herring, sprat and common eider (ΣPBDE 0.3-2.0 ng g⁻¹ ww), while the levels were higher in the herring gull samples (ΣPBDE 1.3-29.9 ng g⁻¹ ww). Hexa-decaBDEs were also found in samples from herring gulls. Eggs from herring gulls from the sub-Arctic contained four times more PBDE than the Swedish herring gulls eggs. Fish samples from the Arctic had two times higher levels of PBDEs and DDTs than similar samples from Sweden. The higher levels of contaminants in fish and seabirds from the Arctic reflect differences in transport processes, feeding ecology (reflected by trophic levels) and metabolism. PBDEs contributed to <10% of the total contaminant load in all investigated samples. The relative contribution of DDTs was higher in fish and bird samples from the Arctic when compared to Swedish samples, e.g. 65% in glaucous gull livers compared to 10% in herring gull livers. This study shows that even though the Swedish west coast is more urban than the Arctic, higher pollutants levels are found in seabird species from the Arctic.     

Residues of chlorinated pesticides in the eggs of Karelian birds, 1989-90

Eggs (n = 52) of four aquatic bird species (Larus canus, Larus argentatus, Larus ridibundus, Sterna hirundo) and crow (Corvus cornix), collected in Southern Karelia in 1989 and 1990, contained DDE and lindane. The highest mean levels of these pollutants were in herring gull eggs and in common tern eggs. The lowest mean levels of pesticides were in crow eggs. In all eggs, DDE concentrations were lower than the critical threshold and it seems, cannot influence reproductive success.     

Polychlorinated biphenyls in diseased lesser black-backed gull (Larus fuscus fuscus) chicks from the Gulf of Finland

Diseases due to the degeneration of the liver and various other internal organs were the major cause of the exceedingly high chick mortality in lesser black-backed gulls (Larus fuscus fuscus) in the central Gulf of Finland, Baltic Sea, during 1991-1993. The same symptoms were found in chicks of common gulls (Larus canus) and herring gulls (Larus argentatus) from the same focal area, although at a much lower frequency. We found disproportionately high concentrations of polychlorinated biphenyls (PCBs) in liver relative to leg muscle in lesser black-backed chicks compared with common gull and herring gull chicks. The causality between PCB residues and chick diseases remains unknown. No signs of chick edema disease or abnormal frequency of embryonic deaths, commonly associated with organochlorines in biota, were found. It is concluded that studies made in a very small geographical area may not give a good correlation between dose and effect due to an even greater variation in tolerance. Another explanation is that the diseases may not have been PCB-induced.     

Organochlorine concentrations in diseased vs. healthy gull chicks from the northern Baltic

The population decline of the nominate lesser black-backed gull Larus fuscus fuscus in the Gulf of Finland (northern Baltic) is caused by an exceedingly high chick mortality due to diseases. The chick diseases include degeneration in various internal organs (primarily liver), inflammations (mainly intestinal), and sepsis, the final cause of death. The hypothesis of starvation causing intestinal inflammations (leading to sepsis) was tested by attempting to reproduce lesions in apparently healthy herring gull L. argentatus chicks in captivity. The herring gull chicks were provided a similar low food-intake frequency as observed for the diseased chicks in the wild. However, empty alimentary tract per se did not induce the intestinal inflammations and therefore, inflammations seem to be innate or caused by other environmental factors in the diseased lesser black-backed chicks. They had very high concentrations of PCB in their liver; but the concentrations were not significantly higher than those of the healthy herring gull chicks, indicating a common exposure area for both species (i.e. the Baltic Sea). When compared to NOEL and LOEL values for TEQs in bird eggs our TEQ levels clearly exceed most or all of the values associated with effects. Compared with published data on fish-eating waterbirds, the DDE concentrations in the diseased lesser black-backed chicks were well above the levels previously correlated with decreased reproduction, while the residues in apparently healthy herring gulls were below those levels. The DDE/PCB ratio in lesser black-backs was significantly elevated, indicating an increased exposure to DDTs as compared with most other Baltic and circumpolar seabirds. The possible exposure areas of DDT in relation to differential migration habits of the two gull species are discussed.     

Mercury levels in Great Lakes herring gull (Larus argentatus) eggs, 1972-1992

Since 1971, the herring gull (Larus argentatus) has been used as a sentinel species for monitoring the levels of persistent contaminants in the Great Lakes ecosystem. In this study, 21 herring gull colonies in the Great Lakes and connecting channels were sampled during 1972-1976, 1981-1983, 1985 and 1992. For each year, 10 eggs (usually) were collected from each colony site and analyzed for total mercury (microg/g, wet wt). Results indicated that eggs from Lake Ontario displayed the highest lake-wide mercury levels (0.28-0.73 microg/g), followed by Lake Superior (0.21-0.50 microg/g). Lake Erie typically displayed the lowest mercury levels (0.18-0.24 microg/g). Overall, mercury levels ranged from 0.12 microg/g in 1985 to 0.88 microg/g in 1982 for Channel Shelter Island (Lake Huron) and Pigeon Island (Lake Ontario), respectively. Generally, all colony sites showed peak egg mercury levels in 1982. A significant decline in egg mercury levels was observed in five colony sites for the period 1972-1992 and in three different colony sites for the period 1981-1992. Mercury levels in the eggs of herring gulls for the period of this study were below levels associated with acute toxic effects in this species but were within a range, for certain years, which potentially reduces hatchability in other avian species.     

EROD activity and stable isotopes in seabirds to disentangle marine food web contamination after the Prestige oil spill

In this study, we measured via surgical sampling hepatic EROD activity in yellow-legged gulls from oiled and unoiled colonies, 17 months after the Prestige oil spill. We also analyzed stable isotope composition in feathers of the biopsied gulls, in an attempt to monitor oil incorporation into marine food web. We found that yellow-legged gulls in oiled colonies were being exposed to remnant oil as shown by hepatic EROD activity levels. EROD activity was related to feeding habits of individual gulls with apparent consequences on delayed lethality. Capture-recapture analysis of biopsied gulls suggests that the surgery technique did not affect gull survival, giving support to this technique as a monitoring tool for oil exposure assessment. Our study highlights the combination of different veterinary, toxicological and ecological methodologies as a useful approach for the monitoring of exposure to remnant oil after a large oil spill.     

Atrazine induction of cytochrome P450 in Chironomus tentans larvae

Cytochrome P450-dependent aldrin epoxidation was characterized in third instar larvae of the aquatic midge, Chironomus tentans. Optimal in vitro assay conditions for the epoxidase were pH 7.6 and 31 degrees C. Activity was linear up to 40 min of incubation time and 0.5 mg microsomal protein per incubation. The activity was concentrated in the microsomal fraction of whole body homogenates and was NADPH-dependent. The effect of atrazine exposure on aldrin epoxidase was measured to determine if this herbicide induces cytochrome P450-dependent activity. Comparisons of control and atrazine-exposed midges indicated increased epoxidase activity as a result of atrazine exposure, and a 45 kDa protein of increased intensity was observed after SDS-PAGE of microsomal protein. The molecular weight of this protein was similar in size to cytochrome P450 enzymes reported for other insects. Heme staining of SDS-PAGE gels and immunochemical studies using a Drosophila melanogaster anti-P450 polyclonal antiserum, further support the cytochrome P450 nature of this inducible 45 kDa protein.     

Levels of DDT and PCB's in different stages of life cycle of the Arctic tern Sterna paradisaea and the herring gull Larus argentatus

∑DDT and PCB levels were analysed in samples of arctic terns and herring gulls collected in the archipelago of southwestern Finland. Special attention was paid to the levels at various stages of the life cycle and in different sexes. The levels were nearly ten times higher in the herring gull. The highest loads were found in adult birds and in newly hatched chicks but the levels were much lower (only 7–12 % in the herring gull) in chicks just before fledgling. The levels in young gulls remained low until the end of August at least. Therefore it is plausible that the high levels found in adult gulls are a consequence of their wintering in the southern Baltic.The levels of ∑DDT and PCB residues were significantly lower in female arctic terns than in male terns. Differences between the sexes were small in the herring gull. Thus it is possible that the female of the arctic tern is able to release pollutants, especially PCB residues, more effectively into eggs than the female of the herring gull. The biochemical mechanisms involved are not clear but a possible explanation may be different lipoprotein structures in the eggs of the species.     

Metal accumulation in tissues of seabirds from Chaun, northeast Siberia, Russia

Concentrations of four essential elements (Fe, Mn, Zn, and Cu) and two toxic metals (Cd and Hg) were determined in selected tissues of 11 seabird species collected in Chaun, northeast Siberia. In oldsquaw, arctic tern and herring gull, zinc concentrations were correlated with Cd concentrations. Cadmium concentrations in all the species were highest in kidney and Hg in liver. Cd levels in the liver and kidney of herring gulls were higher than those observed from other breeding areas. Similarly, Hg concentrations were also high in the liver of herring gull. High concentrations of Cd and Hg found in some birds from Chaun might have arisen from exposure on migration.     

Monitoring organic contaminants in eggs of glaucous and glaucous-winged gulls (Larus hyperboreus and Larus glaucescens) from Alaska

Gull eggs have been used to monitor contaminants in many parts of the world. The Seabird Tissue Archival and Monitoring Project (STAMP) is a long-term program designed to track trends in pollutants in northern marine environments using seabird eggs. Glaucous and glaucous-winged gull (Larus hyperboreus and Larus glaucescens) eggs collected in 2005 from seven Alaskan colonies were analyzed for organic contaminants. Concentrations ranged from below detection limits to 322 ng g⁻¹ wet mass in one egg for 4,4′-DDE and differed among the samples collected in the Gulf of Alaska and Bering and Chukchi Seas. Chick growth and survival rates may be affected by the contaminant levels found in the eggs, but the eggs should be safe for human consumption if they are eaten in small quantities. STAMP plans to continue collecting and banking gull eggs for future real-time and retrospective analyses.     

Extinction risk to bird populations caused by DDT exposure

The impact of toxic chemicals on wild animals and plants can be quantified in terms of the enhanced risk of population extinction. To illustrate a method for doing this, we estimated such impact for two bird species: herring gull (Larus argentatus) in Long Island, NY, and sparrowhawk (Accipiter nisus) in eastern England, when they were exposed to DDT (p,p(')-dichlorodiphenyltrichloroethane) and its metabolites (called DDTs). The method we used is based on a formula of the mean time to population extinction derived for a stochastic differential equation (the canonical model). The intrinsic rate of natural population growth was estimated from an exponentially growing population, and the intensity of the environmental fluctuation was estimated from the magnitude of population size fluctuation. The effect of exposure to DDTs in reducing the population growth rate was evaluated based on an age-structured population model, by assuming that age-specific fertility is density-dependent and sensitive to DDTs exposure, but age-specific survivorship is not. The results are expressed in terms of the risk equivalent--the decrease in carrying capacity K that causes the same enhancement of extinction risk as chemical exposure at a given level. The risk equivalent can be used in mitigation banking.     

Assessment of Blue Mussel <Emphasis Type="Italic">Mytilus edulis</Emphasis> Fisheries and Waterbird Shellfish-predator Management in the Danish Wadden Sea

We assessed the blue mussel Mytilus edulis fishery management scheme introduced in 1994 in the Danish Wadden Sea that regulate fishing vessels, fishery quota, set-aside for mussel-eating birds and established zones closed to mussel fishery. The results showed (i) a reduction in the blue mussel biomass and mussel bed areas in zones closed to fishery, (ii) decrease in eiders Somateria mollissima numbers and increase or stable numbers for oystercatcher Haematopus ostralegus and herring gull Larus argentatus and (iii) that energy estimations based on ecological food requirements for the mussel-eating birds should be at least three times larger, than the amount set-aside in the mussel management scheme. It is concluded that the mussel management scheme had been unable to stabilize or increase the blue mussel stocks and to secure stable or increasing numbers for all target bird species. Thus, it is recommended to revise the present blue mussel management scheme in the Danish Wadden Sea, to continue and improve mussel stock and bird surveys, and to consider novel studies of the mussel-eating birds’ energetics for improved set-aside estimates and future assessments.     

Organochlorine contamination in bird's eggs from the Danube Delta

In this study we report the levels of organochlorine compounds in eggs of aquatic birds from the Danube Delta, a major European wetland. The eggs were collected in 1997 and belonged to the following species: the mallard (Anas platyrhynchos), the greylag goose (Anser anser), the mute swan (Cygnus olor), the coot (Fulica atra), the glossy ibis (Plegadis falcinellus), the spoonbill (Platalea leucorodia), the little egret (Egretta garzetta), the night heron (Nycticorax nycticorax), the grey heron (Ardea cinerea), the great white egret (Egretta alba), the red-necked grebe (Podiceps griseus), the Dalmatian pelican (Pelecanus crispus), the Pygmy cormorant (Phalacrocorax pygmaeus) and the common cormorant (Phalacrocorax carbo). Dichlorodiphenyltrichloroethane (DDT) levels were higher in eggs of the little egret, the great white egret, the cormorant and the Pygmy cormorant with respect to the other species (48,399, 13,613, 12,400 and 10,417 ng/g dry wt., respectively). Hexachlorobenzene (HCB) levels were lower than 1393 ng/g dry wt. in all species while polychlorinated biphenyl (PCB) concentrations in the Pygmy cormorant (2565 ng/g dry wt.) were higher than in the other species. The toxicity evaluation was based on 2,3,7,8-TCDD toxic equivalent factors (TEF) and non-ortho PCB congeners contributed much more than mono-ortho PCBs in most of species. A further aim of this study was to evaluate the possible differences of organochlorine levels in bird eggs collected in the same area in 1982 and in 1997; generally speaking the levels detected in the latter period were lower than those detected in the earlier one.     

Perfluorinated and chlorinated pollutants as predictors of demographic parameters in an endangered seabird

Despite global occurrence of several perfluorinated compounds (PFCs) the potential ecological effects of such substances on natural populations are not known. In endangered lesser black-backed gulls (Larus fuscus fuscus) on the Norwegian Coast, the blood concentrations of PFCs were as high as legacy organochlorines (OCs), and here we examined whether PFCs show associations similar to those of OCs to factors potentially affecting population growth, by evaluating relationships between contaminant concentrations and demographic parameters (reproductive performance and the probability of adults returning between breeding seasons). PFCs were not adversely associated with demographic parameters, while the most persistent OCs; notably PCB and p,p′-DDE, were adversely associated with early chick survival, and adult return rate. This study thus suggests that when the concentrations of PFCs and OCs are of similar magnitude in a gull population, OCs are more likely to cause adverse ecological effects.     

Persistent organic pollutants,heavy metals and parasites in the glaucous gull (Larus hyperboreus) on Spitsbergen

The prediction of a higher parasite infection as a consequence of an impaired immune system with increasing persistent organic pollution (POP) and heavy metal levels were investigated in adult glaucous gull (Larus hyperboreus) from Svalbard. The levels of chlorinated pesticides, polychlorinated biphenyls (PCBs), toxaphenes and polybrominated diphenyl ethers (PBDEs) were measured in liver. Cupper, cadmium, lead, mercury, selenium and zinc were measured in kidney samples. An elevated ratio of PCB-118 was found, suggesting that local contamination from the settlement was detectable in the glaucous gull. Eight cestodes, four nematodes, two acanthocephalan and three trematode helminth species were found in the intestine. A positive correlation was found between cestode intensities and selenium levels and between acanthocephalan intensities and mercury levels. No correlation was found between parasite intensities and POP concentrations. It is concluded that the contaminant levels found in glaucous gulls do not cause immune suppression severe enough to affect parasite intensity.     

Environmental pollutants in endangered vs. increasing subspecies of the lesser black-backed gull on the Norwegian Coast

Organochlorine (OC) residues were measured in eggs and blood of different subspecies of the lesser black-backed gull, Larus fuscus, on the Norwegian coast: a) increasing L. f. intermedius in the North Sea; b) endangered L. f. fuscus near the Arctic Circle; c) L. f. fuscus and greyish-mantled gulls, with a L. f. intermedius appearance, in the Barents Sea region. The dominating OCs in lesser black-backed gulls were polychlorinated biphenyls (PCB) and p,p'-dichlorodiphenyldichloroethylene (DDE). DDE and beta-hexachlorocyclohexane (beta-HCH) residues were higher in L. f. fuscus compared to L. f. intermedius and greyish-mantled birds in the Barents Sea region. In the latter area, blood residues of PCB and DDE in lesser black-backed gulls were as high as in great black-backed gulls, Larus marinus, while in the other regions they were lower. The higher DDE residues in endangered L. f. fuscus compared to increasing L. f. intermedius and greyish-mantled birds, which are invading northern Norway, suggest that OCs may have played a role in the population decline of L. f. fuscus, possibly in combination with nutrient stress.     

Polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecane (HBCD) in seven different marine bird species from Iceland

Data on distribution, concentration and trends of polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecanes (HBCDs) is scarce in biota from the sub-Arctic region of the Atlantic. The present study is an investigation on PBDE and HBCD concentrations in eggs from seven marine bird species from Iceland, i.e. common eider (Somateria mollissima), arctic tern (Sterna paradisaea), guillemot (Uria aalge), fulmar (Fulmarus glacialis), lesser black-backed gull (Larus fuscus), great black-backed gull (Larus marinus) and great skua (Stercorarius skua). Concentrations of sum PBDEs ranged from 44 ng g⁻¹ fat in eider eggs to 2400 ng g⁻¹ fat in great skua eggs. The contribution of different PBDE congeners to the sum concentration differed between species. Concentration of HBCDs (sum of α−,β⁻ and γ−HBCD) ranged from 1.3 ng g⁻¹ fat in arctic tern eggs to 41 ng g⁻¹ fat in great black-backed gull. PCA on PBDE and HBCD shows different trends between the two BFR groups, further indicating different sources/usage. Investigations on any potential health or population effects of environmental pollutants on the great skua are advised since both the PBDE and HBCD concentrations are high.     

Radionuclides and the birds at Ravenglass

Since 1983, concern has been expressed about the apparent decline in numbers of birds in the Ravenglass estuary in west Cumbria, particularly of the black-headed gull colony on the Drigg dunes, and suggestions have been made that this decline might be due to excessive radiation in the birds' food and their general environment. Twelve species of marine invertebrates from Ravenglass, most of them known to be important foods for birds, were analysed, and further samples were taken from sites along the west Cumbrian coast. None of these samples showed excessive contamination with any of the radionuclides analysed. Analysis of a sample of bird carcasses from the areas showed oystercatchers (Haematopus ostralegus) and shelduck (Tadorna tadorna) to have some of the highest concentrations of (137)Cs in their tissues; yet their breeding success and populations were not affected. Black-headed gulls, on the other hand, were found to be feeding mainly inland, and were the least contaminated with radionuclides of all the birds at Ravenglass, yet this species and its breeding success were in decline. Calculations of the total dose equivalent rate to the whole body of the most contaminated black-headed gull amounted to 9.8 x 10(-4) mSvh(-1) (approximately equal to 8.4 x 10(-4) mGy h(-1), whole body absorbed dose rate), and the background exposure dose was of the order of 8.3 x 10(-4) mGy h(-1). As a minimum chronic dose of 1000 mGy day(-1) has been found necessary to retard growth of nestling birds, and 9600 mGy over 20 days of incubation to cause the death of 50% of embryos in black-headed gulls' eggs, the concentrations of radionuclides in the foods, body tissues and general environment were at least three orders of magnitude too low to have had any effect. The more likely cause of the desertion of the gullery was the combination of an uncontrolled fox population, the severest outbreak of myxomatosis amongst the rabbits since 1954 and the driest May-July period on record, all in the same year (1984).     

Organochlorine contaminants in eggs of the yellow-legged gull (Larus cachinnans michahellis) in the North Eastern Mediterranean: is this gull a suitable biomonitor for the region?

Levels of eight PCB congeners and thirteen organochlorine pesticides were measured in eggs sampled at four yellow-legged gull colonies from the Aegean Sea (NorthEastern Mediterranean) in 1997. There were no significant differences among colony areas in the median concentrations in any of the pollutants whereas cluster analyses did not generally reveal reasonable pollution patterns. The maximum concentrations of four congeners were found at Kinaros colony and of nine compounds were found at Lipsos colony. Fingerprints in both groups were similar in all areas. Of PCBs, congener 28, 118, 138, 180 and of pesticides beta-BHC and 2,4'-DDD were prominently dominant suggesting a particular pollution pattern in this region. Statistically significant correlations were found between most of the higher PCBs in all areas studied. The DDT metabolites correlated mostly with other OCs. We suggest that regional pollution by both groups is not adequately reflected in the eggs of this gull probably due to its extensive scavenging habits and, though information is needed from more colonies, it seems to be a poor biomonitor for organochlorines in this region.