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.

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.

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.

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.

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.

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.

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.

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, 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 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 in feathers of Audouin's gull (Larus audouinii) chicks from northeastern Mediterranean colonies.

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 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.

The interactive effects of age and food supply on the breeding ecology of great skuas.

Age-specific variation in the reproductive performance of great skuas in Shetland, U.K., was investigated during a period of fluctuating sandeel availability between 1988 and 1993. Increased sandeel abundance was associated with earlier laying dates, increased clutch volumes and improved fledging success. Sandeel abundance had no effects on clutch size and hatching success. Parental age improved haying date and clutch size in a nonlinear manner. Laying date became earlier in the youngest age classes, with the effect being negligible in older birds. Clutch size increased with age up to 18 and then declined in older birds. Clutch volume increased with age and the probability of nest predation declined with age. There were no significant interactive effects of age and year on laying date nor clutch volume, indicating that birds of all ages benefited equally from increases in sandeel abundance. This suggests that lack of breeding experience rather than deficient foraging skills are responsible for young birds laying later. There was a significant interactive effect of year and age on fledging success that was associated with changes in sandeel availability. Success was uniformly low for birds of all ages in 1988-90 when sandeel abundance was low. Success increased with age in 1991 and 1992 during which time food supply improved. During 1993 food supply was abundant and fledging success was high in all age classes. Age-specific improvements in laying date, clutch size and nest predation were best explained by learning of skills associated with experience of breeding. Improvements in fledging success with age were probably best explained by the learning of skills associated with foraging.

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.

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.

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.

Relationships between heavy metal and metallothionein concentrations in lesser black-backed gulls, Larus fuscus, and Cory's shearwater, Calonectris diomedea.

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.