Hemispheric asymmetry in ocean change and the productivity of ecosystem sentinels.

Climate change and other human activities are causing profound effects on marine ecosystem productivity. We show that the breeding success of seabirds is tracking hemispheric differences in ocean warming and human impacts, with the strongest effects on fish-eating, surface-foraging species in the north. Hemispheric asymmetry suggests the need for ocean management at hemispheric scales. For the north, tactical, climate-based recovery plans for forage fish resources are needed to recover seabird breeding productivity. In the south, lower-magnitude change in seabird productivity presents opportunities for strategic management approaches such as large marine protected areas to sustain food webs and maintain predator productivity. Global monitoring of seabird productivity enables the detection of ecosystem change in remote regions and contributes to our understanding of marine climate impacts on ecosystems.

Sympatric speciation by allochrony in a seabird.

The importance of sympatric speciation (the evolution of reproductive isolation between codistributed populations) in generating biodiversity is highly controversial. Whereas potential examples of sympatric speciation exist for plants, insects, and fishes, most theoretical models suggest that it requires conditions that are probably not common in nature, and only two possible cases have been described for tetrapods. One mechanism by which it could occur is through allochronic isolation-separation of populations by breeding time. Oceanodroma castro (the Madeiran or band-rumped storm-petrel) is a small seabird that nests on tropical and subtropical islands throughout the Atlantic and Pacific Oceans. In at least five archipelagos, different individuals breed on the same islands in different seasons. We compared variation in five microsatellite loci and the mitochondrial control region among 562 O. castro from throughout the species' range. We found that sympatric seasonal populations differ genetically within all five archipelagos and have ceased to exchange genes in two. Population and gene trees all indicate that seasonal populations within four of the archipelagos are more closely related to each other than to populations from the same season from other archipelagos; divergence of the fifth sympatric pair is too ancient for reliable inference. Thus, seasonal populations appear to have arisen sympatrically at least four times. This is the first evidence for sympatric speciation by allochrony in a tetrapod, and adds to growing indications that population differentiation and speciation can occur without geographic barriers to gene flow.

Plastic debris in great skua (Stercorarius skua) pellets corresponds to seabird prey species.

Plastic is a common item in marine environments. Studies assessing seabird ingestion of plastics have focused on species that ingest plastics mistaken for prey items. Few studies have examined a scavenger and predatory species that are likely to ingest plastics indirectly through their prey items, such as the great skua (Stercorarius skua). We examined 1034 regurgitated pellets from a great skua colony in the Faroe Islands for plastics and found approximately 6% contained plastics. Pellets containing remains of Northern fulmars (Fulmarus glacialis) had the highest prevalence of plastic. Our findings support previous work showing that Northern fulmars have higher loads of plastics than other sympatric species. This study demonstrates that marine plastic debris is transferred from surface feeding seabird species to predatory great skuas. Examination of plastic ingestion in species that do not ingest plastics directly can provide insights into how plastic particles transfer vertically within the food web.

Increased reproductive effort results in male-biased offspring sex ratio: an experimental study in a species with reversed sexual size dimorphism.

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.

Enigmatic phylogeny of skuas (Aves:Stercorariidae)

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.

The chemical form of mercury stored in South Atlantic seabirds.

Concentrations of total mercury and organic (methyl) mercury were measured in the liver tissue of adults of 12 seabird species collected at colonies on Gough Island, South Atlantic Ocean. Total mercury levels showed both great intra- and interspecies variation, ranging from a mean of 1343.0 microg g(-1) dry weight in wandering albatrosses to a mean of 0.8 microg g(-1) dry weight in broad-billed prions. Organic mercury levels were less variable both between, but especially within, species. Organic mercury levels, expressed as a percentage of total mercury levels, ranged from a mean of 2.6% in wandering albatrosses up to a mean of 92.6% in littee shearwaters. Within each species, individuals with the highest total mercury levels tended to have the lowest percentage organic mercury, this trend being statistically significant in several species. Two species exhibited a significant positive correlation between organic mercury levels, in absolute terms, and total mercury levels. When all 12 species were considered, a highly significant negative correlation between mean percentage organic mercury and mean total mercury was found (rs = -0.888, P < 0.001). These results provide evidence to suggest that some seabirds may be capable of demethylating organic mercury in a species-dependent and that eliminatory pathways for the excretion of dietary mercury may influence the mode of response of a particular species.

Mercury in feathers of Squacco Heron (Ardeola ralloides) chicks in relation to age, hatching order, growth, and sampling dates.

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.

Mercury levels in the plumage of red-billed gulls Larus novaehollandiae scopulinus of known sex and age.

Samples of 4-8 small body feathers were taken from 27 chicks and 35 adult red-billed gulls caught at their nests on the Kaikoura Peninsula, New Zealand, in December 1988. The adults had been ringed as chicks and were of known ages from 2 to 15 years old. Analysis of total mercury in the feather samples showed that levels were independent of sex and age in adults. Mean fresh weight concentration in adult body feathers was 2.4 microg g(-1). The lack of age accumulation of mercury in gull feathers contrasts with the well known age related accumulation of mercury in tissues of fish and marine mammals, but agrees with predictions of recent studies on mercury dynamics in birds. Mercury levels in chick feathers were about 80% of levels in adult feathers.

Mercury levels in eggs, tissues, and feathers of herring gulls Larus argentatus from the German Wadden Sea Coast.

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.

Feathers as a means of monitoring mercury in seabirds: Insights from stable isotope analysis.

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.

Metal concentrations in seabirds of the New Zealand region.

Concentrations of the heavy metals cadmium, copper, lead, zinc, mercury and, in some individuals, methyl mercury were determined in a range of tissues of 64 tropical, subtropical, subantarctic and antarctic seabird taxa mostly from the New Zealand region. Although apparently natural, levels of cadmium and mercury in some species greatly exceed those known to have toxic effects in some terrestrial birds. Copper and zinc levels exhibited less inter-species variation than the non-essential metals cadmium and mercury. Cadmium concentrations were highest in kidney tissues but uniformly low in feathers. Total mercury concentrations showed most inter-species variation. Mean methyl mercury levels in liver tissues of several large procellariiforms represented less than 5% of the corresponding mean total mercury level. Lead concentrations were generally low or below the limits of detection, but elevated levels were measured in some coastal or scavenging species. In a significant number of species, mean concentrations of liver cadmium and mercury and kidney cadmium were greater in adults than in young birds. The reverse was true for copper. Mean zinc levels in liver did not differ between adults and young. High levels of cadmium in some species seem likely to be due to diet, whereas high levels of mercury probably reflect more closely the moult intervals which constrain the ability of birds to eliminate methyl mercury.

Metallothionein induction and condition index of dogwhelks Nucella lapillus (L.) exposed to cadmium and hydrogen peroxide.

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.

Kinetics, dose-response, excretion, and toxicity of methylmercury in free-living Cory's shearwater chicks.

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.

Survival, growth, metallothionein and glycogen levels of Nucella lapillus (L.) exposed to subchronic cadmium stress: the influence of nutritional state and prey type.

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.

Great skua (Stercorarius skua) movements at sea in relation to marine renewable energy developments.

Marine renewable energy developments (MREDs) are an increasing feature of the marine environment. Owing to the relatively small number of existing developments and the early stage of their associated environmental monitoring programmes, the effects of MREDs on seabirds are not fully known. Our ability to fully predict potential effects is limited by a lack of knowledge regarding movements of seabirds at sea. We used GPS tracking to improve our understanding of the movements at sea of a protected seabird species breeding in Scotland, the great skua (Stercorarius skua), to better predict how this species may be affected by MREDs. We found that the overlap of great skuas with leased and proposed MREDs was low; particularly with offshore wind sites, which are predicted to present a greater risk to great skuas than wave or tidal-stream developments. Failed breeders overlapped with larger areas of MREDs than breeding birds but the overall overlap with core areas used remained low. Overlap with wave energy development sites was greater than for offshore wind and tidal-stream sites. Comparison of 2011 data with historical data indicates that distances travelled by great skuas have likely increased over recent decades. This suggests that basing marine spatial planning decisions on short-term tracking data could be less informative than longer-term data.

The role of eggs in mercury excretion by Quail Coturnix coturnix and the implications for monitoring mercury pollution by analysis of feathers.

: This paper describes differences in the excretion of methyl mercury between male and female Quail Coturnix coturnix after a single dose. Since feathers are often used to monitor mercury pollution it is important to take into account biases in feather mercury levels that may arise as a result of mercury loss through egg-laying. Evidence is presented to support the use of bird eggs to sample for environmental mercury contamination. Birds were monitored up to twelve weeks after administration. Mercury concentrations in the kidney exceeded those in the liver which exceeded those in the pectoral muscle. Significant differences in mercury levels between male and female birds were found up to eight weeks after administration. Mercury was initially distributed through most of the internal tissues and was lost relatively slowly in a negative exponential manner. Mercury loss through excretion differed between the sexes for the first eight weeks after mercury administration. Initial mercury concentration in eggs was 3.5 µg g(-1) but no mercury was detected in eggs five weeks after the dose was administered. At this point over 40% of the females' intake had been lost into the eggs.

Kinetics, dose--response, and excretion of methylmercury in free-living adult Cory's shearwaters.

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.

Mercury in feathers of little egret Egretta garzetta and night heron Nycticorax nycticorax chicks and in theirprey in the Axios Delta, Greece.

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.

Induction of metallothionein in dogwhelk Nucella lapillus during and after exposure to cadmium.

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.