Variation of mercury contamination in chicks of little Tern Sterna albifrons in southwest Europe: brood, age, and colony related effects.
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Biomedical subjects
Publications and source records attributed to R W Furness.
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Adaptive sex-ratio theory predicts that parents should overproduce the more beneficial offspring sex. Based on a recent experimental study of lesser black-backed gulls, we tested this hypothesis with the great skua, Catharacta skua, a bird species closely related to gulls but where females are the larger sex. When in poor body condition, the gulls overproduced daughters, the smaller and more viable sex under those circumstances. To discriminate between a mandatory physiological overproduction of female (i.e. non-male) eggs versus the overproduction of the smaller and presumably more viable sex, we conducted an egg-removal experiment with the great skua. Since the males are smaller, larger size and being male are separated. Through egg removal we induced females to increase egg production effort. Eggs were sexed using a DNA-based technique. Manipulated pairs produced a significant male bias at the end of the extended laying sequence, while the sex ratio in the control group did not differ from unity. Our results present an example of facultative sex-ratio manipulation and support the hypothesis that in sexually dimorphic birds parents overproduce the smaller sex under adverse conditions.
We evaluated methylmercury (MHg) kinetics, dose--responses, and excretion in free-living adult Cory's shearwaters using a nondestructive multi-tissue approach. Elimination of MHg in blood comprised an initial fast phase, with half-time of 1 d, and a slow terminal phase with half-time between 44 and 65 d. Molt was a crucial factor in determining the rate of MHg elimination. Half-times were independent of dose. A relationship between steady-state blood concentrations and dietary intake of MHg was derived. Ratios between Hg concentrations in eggs or hatchlings' plumage and parental blood were independent of dose, with tissue--blood partition coefficients identical to those in controls. Dose--response relationships were linear. Females were subjected to Hg concentrations 18% higher than males but exhibited a 10% lower dose--response in blood. The difference is not fully accounted for by excretion into the egg and may be due to unidentified sex-related differences in physiology. Excretion rates into plumage showed no dose dependency but were higher (33% of intake) in birds exposed during molt than in birds dosed 2 months before the start of molt. Hg excretion through the skin in exfoliated epidermal cells that adsorb into plumage was estimated to represent 8% of the intake. The results of this study may be used in advanced modeling of the kinetics of MHg in adult birds to fill the current gap of a bioenergetic model for avian exposure to MHg.
It has been suggested that metallothionein (MT) not only can regulate essential metals and detoxify toxic metals, but that MT can also play a significant role as an antioxidant and can be induced by oxidative stresses other than metals. This study is aimed at investigating the effect of hydrogen peroxide (H2O2), and the combined effect of H2O2 and cadmium (Cd) on MT induction and condition index (CI) in dogwhelks Nucella lapillus. Adult male dogwhelks (27 +/- 1 mm in shell length) were exposed for 20 days to (1) control (filtered natural seawater only); (2), 0.50 ppm Cd; (3) 2.0 ppm H2O2 + 0.50 ppm Cd; (4) 1.0 ppm H2O2 + 0.25 ppm Cd; (5) 2.0 ppm H2O2; (6) 1000 ppm H2O2 or (7) 1000 ppm H2O2 + 0.50 ppm Cd. The concentration of MT in the Leiblein gland of N. lapillus was quantified using the silver saturation method. MT or MT-like proteins in the animals were induced by Cd (0.5 ppm), H2O2 (2.0 ppm) or Cd + H2O2, indicating that MT in this gastropod species can be induced by either metal or oxidative stresses. Exposure to high H2O2 (1000 ppm) alone or combined with Cd, and exposure to Cd (0.50 ppm) or H2O2 (2.0 ppm), resulted in significant weight loss, indicated by a reduction of CI. However, CIs of groups (3) and (4) were similar to that of the control suggesting that Cd antagonistically reduces toxicity caused by H2O2 since Cd-induced MT may have a protective function against hydroxyl radicals.
Dogwhelks Nucella lapillus feed mainly on mussels and barnacles, and may experience periods of starvation. We report effects of nutritional state and prey type on the survival, growth, cadmium (Cd) accumulation, metallothionein (MT) induction and glycogen stores in N. lapillus exposed to Cd in water. Adult dogwhelks, with similar shell length (30.0+/-1.5 mm), were either starved or fed to satiation with barnacles Semibalanus balanoides, mussels Mytilus edulis or Cd-dosed M. edulis, and kept in filtered natural seawater (< 0.01 microg Cd 1(-1)) or Cd-contaminated (400 microg Cd 1(-1)) seawater for 80 days. Mortality and individual growth rate were determined. Cd, MT and glycogen were measured in different tissues. Prolonged starvation and exposure to Cd significantly reduced the survivorship of N. lapillus, but feeding could help dogwhelks to combat Cd toxicity and minimise mortality. Extended starvation also caused tissue wastage, leading to higher concentrations of Cd and MT in tissues, whereas fed animals increased in weight and had lower Cd and MT concentrations because of the tissue dilution effect. Prey type significantly affected growth rate of dogwhelks and indirectly influenced Cd accumulation, MT induction and glycogen stores. Eating mussels promoted better growth and higher glycogen reserves than eating barnacles. Individual growth rate decreased with increasing Cd accumulation. Cd-exposed survivors grew faster and consumed more than control animals, implying that these survivors may have better fitness and greater tolerance to Cd toxicity. The use of growth, condition index, MT and glycogen as biomarkers of environmental pollution are discussed. These results indicate a need to incorporate biological data including growth (or at least condition index) and prey type into biomonitoring programmes to allow sound interpretation.
We studied the relationships between mercury content of Squacco Heron (Ardeola ralloides) chick body-feathers and nestling age, hatching order (seniors-juniors) and growth parameters, and the date of feather sampling in the Axios Delta, northern Greece, in 1993 (n = 75 chicks) and 1994 (n = 80). Mercury levels were not significantly correlated with chick age in either year of the study. Most of the variability in mercury (90%) was found among broods, attributable to differential prey selection and/or foraging habitat and patch utilization by parents. Within broods, juniors had significantly higher mercury loads than seniors in 1993, but there was no significant difference between the two in 1994. Correlations of nestling weight and linear measurements corrected for chick age and mercury concentrations were never significant and explained small amounts of variability in chick growth. However, linear measurements corrected for age were significantly higher among seniors in 1993, when those nestlings had lower mercury loads than their siblings. Mercury levels were unaffected by the date of feather collection in 1993, but exhibited a significant increase over time in 1994. This can be attributed to a shift towards more highly contaminated habitats and prey types by foraging parents, resulting from seasonal changes in water level and vegetation cover in important foraging habitats. Feather collection from Squacco Heron nestlings late in the breeding season seems to be an appropriate method for biomonitoring mercury pollution in the Axios Delta.
Methylmercury (MHg) kinetics, dose-response, excretion, and toxicity were experimentally evaluated and compared between small (one to two weeks old) and large (six to seven weeks old), free-living Cory's shearwater chicks. The half-time for the terminal elimination phase of MHg in blood (5.7 d) and the average percentage of ingested MHg deposited in the blood volume (12%) were independent of the age at exposure. Therefore, these data were employed to derive a relationship between steady-state blood concentrations and dietary intake of MHg in bird chicks. Plumage:blood ratios were independent of dose and could be used as partition coefficients. Dose-response relationships in plumage and blood were linear over the wide range of exposures employed. Blood dose-responses of MHg in small and large chicks were similar. Excretion percentages into the final plumage varied between 42 and 60% of intake. The body condition of experimental chicks did not indicate sublethal toxicity of the doses administered; hence, the exposure levels provide maximum avian no-observed-adverse-effect levels for external symptoms in wild seabird chicks.
Feathers of Audouin's gull chicks from three Aegean island areas (north Dodecanese, Cyclades, Kythera) Greece, were sampled in 1997 and 1998 and analyzed for mercury. Mean concentrations varied from 0. 94 microg/g (Lipsos, Dodecanese, 1998) to 2.14 microg/g (Paros, Cyclades, 1998). Significant differences between years occurred in some regions (Lipsos, Fourni) but not in others (Paros). Within each year, especially in 1998, mean mercury concentrations differed among colonies. Results did not support the prediction that mercury levels would be higher in the north Dodecanese area due to the proximity of the polluted Menderes delta. There was no relationship between estimated chick age and feather mercury contents (r = -0.04, NS). Detected mercury levels do not seem to pose any toxic hazard to the Aegean Audouin's gull populations. However, the ease of sampling from gulls indicates that they may be a useful biomonitor of mercury contamination in this region.
Induction of metallothionein (MT) was investigated in a common biomonitor, the dogwhelk Nucella lapillus (shell length: 27.7+/-1.4 mm; wet tissue weight: 667+/-196 mg), during and after exposure to cadmium (Cd) under controlled laboratory conditions (10+/-1 degrees C and 34+/-1 per thousand salinity). The dogwhelks were exposed to 500 microg Cd l-1 (2.2% of 96 h LC50) for 60 days and then placed into clean seawater for 110 days. MT concentration in whole animal increased during the exposure period, peaked at Day 70, and then declined gradually. Half-life of MT was ca. 40 days. MT concentration increased very significantly with increasing Cd concentration (r=0.74, n=24, P<0.001). Nevertheless, Cd concentration increased throughout the period of exposure and while in clean seawater, leveling off only after Day 120, indicating that Cd concentration could not be regulated by N. lapillus. Throughout the study, MT and Cd concentrations in gills, Leiblein gland, kidney, digestive gland, and gonad tissues increased gradually. Highest concentrations of MT and Cd were found in the Leiblein gland. Measurement of MT induction in the Leiblein gland of N. lapillus may therefore prove useful as a sublethal biological response to Cd contamination.
Mercury concentrations, together with nitrogen and carbon stable isotope signatures, were determined in body feather samples from northern fulmars Fulmarus glacialis and great skuas Catharacta skua, and in different flight feathers from great skuas. There were no significant relationships between trophic status, as defined using isotope analysis, and mercury concentration in the same feather type, in either species. Mercury concentrations in body feather samples were markedly different between fulmars and skuas, reflecting differences in diet, but there was no corresponding difference in trophic status as measured through nitrogen stable isotope signatures. We conclude that mercury concentrations and stable isotope values in feathers are uncoupled, mercury concentrations apparently reflecting the body pool of accumulated mercury at the time of feather growth whilst stable isotope values reflect the diet at the time of feather growth. There were significant positive correlations between the different flight feathers of great skuas for all three parameters measured. These were strongest between primary 10 and secondary 8, suggesting that these two feathers are replaced at the same time in the moult sequence in great skuas. Stable isotope analysis of different feathers may provide a means of investigating moult patterns in birds.
Multiple sources of evidence show that the skuas (Aves:Stercorariidae) are a monophyletic group, closely related to gulls (Laridae. On morphological and behavioural evidence the Stercorariidae are divided into two widely divergent genera, Catharacta and Stercorarius, consistent with observed levels of nuclear and mitochondrial gene divergence. Catharacta skuas are large-bodied and with one exception breed in the Southern Hemisphere. Stercorarius skuas otherwise known as jaegers) are smaller bodied and breed exclusively in the Northern Hemisphere. Evidence from both mitochondrial and nuclear genomes and from ectoparasitic lice (Insecta:Phthiraptera) shows that the Pomarine skua, S. pomarinus, which has been recognized as being somewhat intermediate in certain morphological and behavioural characteristics, is much more closely related to species in the genus Catharacta, especially to the Northern Hemisphere-breeding Great skua, C. skua, than it is to the other two Stercorarius skuas, the Arctic skua, S. parasiticus and the Longtailed skua, S. longicaudus. Three possible explanations that might account for this discordant aspect of skua phylogeny are explored. These involve (i) the segregation of ancestral polymorphism, (ii) convergent evolution of morphology and behaviour or (iii) inter-generic hybridization. The available evidence from both nuclear and mitochondrial genomes does not exclude any of these hypotheses. Thus, resolution of this enigma of skua phylogeny awaits further work.
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Mercury concentrations were measured in feathers oflittle egret and night heron chicks and in their prey in the Axios Delta,Greece. Significantly higher concentrations occurred in night heron than inlittle egret in 1993. In the night heron the mercury content of feathers wasnegatively correlated to the size of chicks, possibly due to inhibition ofgrowth. Mercury concentrations were higher than reported for heron feathersin seriously polluted sites in North America and Japan, but the toxic hazardis unclear. Diets differed considerably between the two species due to use ofdifferent foraging habitats and this seems responsible for different mercurycontents of feathers. Mercury concentrations in the pumpkinseed sunfishLepomis gibbosus, goldfish Carrassius auratus, and indragonfly Odonata larvae were the highest among the prey categories. Frogs and water beetles Dytiscidae had moderate concentrationswhereas saltwater fish and terrestrial prey had very low mercuryconcentrations. The implication is that the deltaic marshes are the habitatmost polluted with mercury. Night heron chick feathers, freshwater fish anddragonfly larvae could be used to monitor mercury contamination in thisregion, but use of bird feathers alone could give misleading results ifchanges in diet occurred.
Metallothionein, cadmium, zinc, copper, and mercury concentrations were measured in adult lesser black-backed gulls, Larus fuscus; and metallothionein, cadmium, zinc, and copper concentrations were measured in fledgling Cory's shearwaters, Calonectris diomedea. In gulls, metallothionein was positively correlated with cadmium (kidney r = 0.83, liver r = 0.46), zinc (kidney r = 0.46, liver r = 0.37), and copper (kidney r = 0.28, liver r = 0.34). Mercury levels in lesser black-backed gulls showed no correlations with metallothionein or with any other metal. In shearwaters metallothionein was positively correlated with cadmium in the kidney (r = 0.41) but not in liver, zinc in kidney (r = 0.43) and liver (r = 0.52), and copper in kidney (r = 0.55) but not in liver. Cadmium levels were the most important factor determining tissue metallothionein concentrations in adult lesser black-backed gulls demonstrating the role of metallothionein in heavy metal detoxification. In fledgling Cory's shearwaters, the most important factor in determining metallothionein concentrations in kidney was copper concentrations, and in liver, zinc concentrations. During the latter phases of chick growth high levels of zinc are required for feather development, and at this time the binding of cadmium may be masked by the presence of a large amount of zinc- and copper-bound metallothionein. These results illustrate disparate roles of metallothionein, the levels of which will be in a state of flux both seasonally and annually.
Eggs, feathers (down, body feathers from side/shoulder and back) and some dead chicks (liver) from broods of three species, herring full (Larus argentatus), black-headed gull (Larus ridibundus), and common tern (Sterna hirundo) from the German North Sea coast were collected to study intersibling differences in mercury contamination and elimination into the growing feathers. The mercury contamination in eggs, feathers, and liver of the terns was about four times that of the gulls; black-headed gulls had lowest mercury concentrations. The body feathers grow when the chicks became older had lower mercury levels than down in the more contaminated species (11% lower in herring gulls, 49% in common terns), indicating the advancing decontamination of the body by the plumage development. The elimination of mercury was greater in chicks with higher mercury levels. Down of the first hatched herring gull and common tern chick contained more mercury than down of the siblings hatched later, because of its higher burden derived from the first laid egg.
Mercury, cadmium, zinc, and copper concentrations were analyzed in three samples of common guillemot (in April, June, and November). Levels measured were uniformly low, and not enough to have any toxic effects. Adult guillemots had significantly more cadmium in their livers and kidneys than juveniles, with juvenile levels ranging from 25% to 89% of adult levels. Mercury concentrations in liver and kidney were also higher in adults. Juvenile levels represented from 80% to 94% of adults, but there were no age differences in feather and muscle mercury. Mercury levels declined throughout the year in internal tissues from April through June to November. There was a strong seasonal fluctuation in cadmium levels in liver and kidney, rising significantly between April and June and declining in both adult and juvenile birds. The influences of seasonal processes (namely breeding and moult) and seasonal dietary differences as causative factors in the changes in metal burdens are discussed. These findings have implications for the use of seabirds as monitors of heavy metals in the marine environment.
The relationships between mercury levels in eggs, tissues, and feathers of male and female herring gulls caught at their nests at a colony on the German Wadden Sea Coast were investigated, and an assessment of mercury intake and excretion of these birds was made. Samples of the liver, ovary, pectoral muscle, and body feathers, as well as the primary feather (in some cases), and eggs were taken from 37 adult herring gulls. Analysis of total mercury in all samples showed that body-feather and tissue levels were independent of sex. There was, however, a significant difference between levels of mercury in the primary feathers of male and female birds. Egg levels were not correlated to pectoral muscle, ovary, or feather levels although they were positively correlated with mercury levels in the liver. Liver levels were in turn correlated with mercury levels in the ovary. The ratio of mean feather to mean egg concentration ranged from 3.7 to 5.5 according to which feather was used. It was estimated that herring gulls from the Wadden coast ingested between 825 and 1337 microg of mercury in the year prior to analysis. It was also estimated that female birds may excrete over 20% more mercury via their eggs than could be excreted by male birds.