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Interspecific and intraspecific variation in organochlorine pesticides and polychlorinated biphenyls using non-destructive samples from Pygoscelis penguins
2021
Souza, Juliana Silva | Pacyna-Kuchta, Aneta Dorota | Teixeira da Cunha, Larissa Schmauder | Costa, Erli Schneider | Niedzielski, Przemysław | Machado Torres, João Paulo
As humans are present in Antarctica only for scientific and tourism-related purposes, it is often described as a pristine region. However, studies have identified measurable levels of Persistent Organic Pollutants (POPs), such as organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs), in the Antarctic region. These are highly toxic anthropogenic compounds with tendency to travel long distances and reach remote environments, where they can bioaccumulate in the biota. Penguins are exposed to POPs mainly through their diet, which they partially eliminate via feathers. Species of the genus Pygoscelis occur around Antarctic continent and its surrounding regions, and can act as indicators of contaminants that reach the continent. Here, we report OCP and PCB levels in feathers of male and female penguins of P. adeliae, P. antarcticus and P. papua from King George Island, South Shetland Islands, Antarctica. Interspecific, sex- and body-size-related differences were investigated in the contamination profiles of PCBs and OCPs. Feather samples were collected from adult penguins (n = 41). Quantification of compounds was performed by gas chromatography-tandem mass spectrometry. The three Pygoscelis species presented similar contamination profiles, with higher concentrations of dichlorodiphenyltrichloroethane (∑DDT; 1.56–3.82 ng g⁻¹ dw), lighter PCB congeners (∑PCB: 11.81–18.65 ng g⁻¹ dw) and HCB (hexachlorobenzene: 1.65–4.06 ng g⁻¹ dw). Amongst the three penguin species, P. antarcticus had lower and P. papua higher concentrations of most of the compounds identified. We found interspecific differences in POPs accumulation as well as sex differences in POP concentrations. Our data indicate a small but significant positive correlation between body size and the concentrations of some compounds. Despite the overall low concentrations found, this study increases knowledge of the occurrence of POPs in Antarctic penguins, thereby reinforcing concerns that Antarctica, although remote and perceived to be protected, is not free from the impact of anthropogenic pollutants.
Show more [+] Less [-]Untangling causes of variation in mercury concentration between flight feathers
2021
Gatt, Marie Claire | Furtado, Ricardo | Granadeiro, José Pedro | Lopes, Daniel | Pereira, Eduarda | Catry, Paulo
Bird feathers are one of the most widely used animal tissue in mercury biomonitoring, owing to the ease of collection and storage. They are also the principal excretory pathway of mercury in birds. However, limitations in our understanding of the physiology of mercury deposition in feathers has placed doubt on the interpretation of feather mercury concentratoins. Throughout the literature, moult sequence and the depletion of the body mercury pool have been taken to explain patterns such as the decrease in feather mercury from the innermost (P1) to the outermost primary feather (P10) of the wing. However, it has been suggested that this pattern is rather a measurement artefact as a result of the increased feather mass to length ratio along the primaries, resulting in a dilution effect in heavier feathers. Here, we attempt to untangle the causes of variation in feather mercury concentrations by quantifying the mercury concentration as μg of mercury (i) per gram of feather, (ii) per millimetre of feather, and (iii) per day of feather growth in the primary feathers of Bulwer’s Petrel Bulweria bulwerii chicks, effectively controlling for some of the axes of variation that may be acting in adults, and monitoring the growth rate of primary feathers in chicks. The mercury concentration in Bulwer’s Petrel chicks’ primaries increased from the innermost to the outermost primary for all three concentration measures, following the order of feather emergence. These observations confirm that the pattern of mercury concentration across primary feathers is not an artefact of the measure of concentration, but is likely an effect of the order of feather growth, whereby the earlier grown feathers are exposed to higher blood mercury concentrations than are later moulted feathers as a result of blood mercury depletion.
Show more [+] Less [-]Year-round element quantification of a wide-ranging seabird and their relationships with oxidative stress, trophic ecology, and foraging patterns
2021
Laranjeiro, Maria I. | Alves, Luís M.F. | da Silva, Joana M. | Pereira, Jorge M. | Norte, Ana C. | Paiva, Vítor H. | Lemos, Marco F.L. | Ramos, Jaime A. | Novais, Sara C. | Ceia, Filipe R.
Multidisciplinary approaches are essential to diligently assess environmental health status of ecosystems. In this study, year-round chemical elements' exposure and impacts were assessed on the wide-ranging Cory's shearwater Calonectris borealis breeding in Berlenga Island, offshore Portugal, North Atlantic Ocean. The aim was to identify potential contamination and oxidative stress sources associated with trophic ecology, habitat and spatial use, and foraging patterns. A set of 20 chemical elements were quantified, along with oxidative stress biomarkers, stable isotope analyses, and GPS tracking data. Birds presented higher accumulation to some non-essential elements along the year (i.e. arsenic, As; cadmium, Cd; mercury, Hg; lead, Pb; and strontium, Sr), in which concentrations were similar or surpassed other procellariform seabird populations all over the world. No significant differences were found for any of the elements between different periods within the breeding season, with exception of Hg. However, a Principal Component Analysis taking into consideration a group of elements showed differences between pre-laying and chick-rearing periods, with overall higher concentrations in the former. Individuals spending more time engaging in an intensive search for food, and in more coastal environments, presented overall higher element concentrations, and particularly Hg. Contrary to expectations, no relationships were found between chemical elements and oxidative stress. On the other hand, spatial use and foraging patterns of Cory's shearwaters influenced their oxidative stress responses. Our results highlight the need for multidisciplinary approaches to deepen understanding of the large-scale vulnerability of bioindicators such as seabirds and, by extension, the overall environmental health of ecosystems in which they rely.
Show more [+] Less [-]Understanding PFAAs exposure in a generalist seabird species breeding in the vicinity of a fluorochemical plant: Influence of maternal transfer and diet
2021
Lopez-Antia, Ana | Kavelaars, Marwa M. | Müller, Wendt | Bervoets, Lieven | Eens, Marcel
Perfluoroalkyl acids (PFAAs) are a focus of scientific and regulatory attention nowadays. However, PFAAs dynamics in the environment and the factors that determine wildlife exposure are still not well understood. In this study we examined PFAAs exposure in chicks of a generalist seabird species, the lesser black-backed gull (Larus fuscus), breeding 49 km away of a PFAAs hotspot (a fluorochemical plant in Antwerp, Belgium). In order to study the pathways of PFAAs exposure, we measured how chicks’ PFAAs burden varied with age, sex, and body condition. In addition, we related PFAA concentrations to chicks’ diet using stable isotope signatures. For this purpose, we studied plasma PFAA concentrations in 1-week and 4-week-old gull chicks. Only 4 (PFOS, PFOA, PFDA and PFNA) out of the 13 target PFAA compounds were detected. Measured concentrations of PFOS and PFOA were generally high compared to other seabird species but were highly variable between individuals. Furthermore, our results suggest that maternal transfer plays a significant role in determining chicks’ PFAAs burden, and that there are variable sources of exposure for PFOS and PFOA during post-hatching development. The association between PFOS and specific stable isotopes (i.e. δ¹⁵N and δ¹³C) suggests a higher exposure to PFOS in birds with a predominantly marine diet. We also found that males’ condition was positively associated with PFOS plasmatic concentration, probably due to the indirect effect of being fed a high quality (marine) diet which appears PFOS rich. Yet, exact exposure source(s) for PFOA remain(s) unclear. Given that PFOS concentrations measured in some chicks surpassed the toxicity reference value calculated for top avian predators, continued monitoring of exposure and health of this gull population, and other wildlife populations inhabiting the area, is highly recommended.
Show more [+] Less [-]Mercury biomagnification in a Southern Ocean food web
2021
Seco, José | Aparício, Sara | Brierley, Andrew S. | Bustamante, Paco | Ceia, Filipe R. | Coelho, João P. | Philips, Richard A. | Saunders, Ryan A. | Fielding, Sophie | Gregory, Susan | Matias, Ricardo | Pardal, Miguel A. | Pereira, Eduarda | Stowasser, Gabriele | Tarling, Geraint A. | Xavier, José C.
Biomagnification of mercury (Hg) in the Scotia Sea food web of the Southern Ocean was examined using the stable isotope ratios of nitrogen (δ¹⁵N) and carbon (δ¹³C) as proxies for trophic level and feeding habitat, respectively. Total Hg and stable isotopes were measured in samples of particulate organic matter (POM), zooplankton, squid, myctophid fish, notothenioid fish and seabird tissues collected in two years (austral summers 2007/08 and 2016/17). Overall, there was extensive overlap in δ¹³C values across taxonomic groups suggesting similarities in habitats, with the exception of the seabirds, which showed some differences, possibly due to the type of tissue analysed (feathers instead of muscle). δ¹⁵N showed increasing enrichment across groups in the order POM to zooplankton to squid to myctophid fish to notothenioid fish to seabirds. There were significant differences in δ¹⁵N and δ¹³C values among species within taxonomic groups, reflecting inter-specific variation in diet. Hg concentrations increased with trophic level, with the lowest values in POM (0.0005 ± 0.0002 μg g⁻¹ dw) and highest values in seabirds (3.88 ± 2.41 μg g⁻¹ in chicks of brown skuas Stercorarius antarcticus). Hg concentrations tended to be lower in 2016/17 than in 2007/08 for mid-trophic level species (squid and fish), but the opposite was found for top predators (i.e. seabirds), which had higher levels in the 2016/17 samples. This may reflect an interannual shift in the Scotia Sea marine food web, caused by the reduced availability of a key prey species, Antarctic krill Euphausia superba. In 2016/17, seabirds would have been forced to feed on higher trophic-level prey, such as myctophids, that have higher Hg burdens. These results suggest that changes in the food web are likely to affect the pathway of mercury to Southern Ocean top predators.
Show more [+] Less [-]Temporal trends and interannual variation in plastic ingestion by Flesh-footed Shearwaters (Ardenna carneipes) using different sampling strategies
2021
Lavers, Jennifer L. | Hutton, Ian | Bond, Alexander L.
The world's oceans are under increasing pressure from anthropogenic activities, including significant and rapidly increasing inputs of plastic pollution. Seabirds have long been considered sentinels of ocean health, providing data on physical and chemical pollutants in their marine habitats. However, long-term data that can elucidate important patterns and changes in seabird exposure to marine pollutants are relatively limited but are urgently needed to identify and support effective policy measures to reduce plastic waste. Using up to 12 years of data, we examined the benefits and challenges of different approaches to monitoring plastic in seabirds, and the relationship between plastic and body size parameters. We found the mass and number of ingested plastics per bird varied by sample type, with lavage and road-kill birds containing less plastic (9.17–9.33 pieces/bird) than beach-washed or otherwise dead birds (27.62–32.22 pieces/bird). Beached birds therefore provide data for only a particular subset of the population, mostly individuals in poorer body condition, including those severely impacted by plastics. In addition, the mass and number of plastics in beached birds were more variable, therefore the sample sizes required to detect a change in plastic over time were significantly larger than for lavaged birds. The use of lavaged birds is rare in studies of plastic ingestion due to ethical and methodological implications, and we recommend future work on ingested plastics should focus on sampling this group to ensure data are more representative of a population's overall exposure to plastics.
Show more [+] Less [-]Within and between breeding-season changes in contaminant occurrence and body condition in the Antarctic breeding south polar skua
2021
Midthaug, Hilde Karin | Hitchcock, Daniel J. | Bustnes, Jan Ove | Polder, Anuschka | Descamps, Sébastien | Tarroux, Arnaud | Soininen, Eeva M. | Borgå, Katrine
The Antarctic ecosystem represents a remote region far from point sources of pollution. Still, Antarctic marine predators, such as seabirds, are exposed to organohalogen contaminants (OHCs) which may induce adverse health effects. With increasing restrictions and regulations on OHCs, the levels and exposure are expected to decrease over time. We studied south polar skua (Catharacta maccormiciki), a top predator seabird, to compare OHC concentrations measured in whole blood from 2001/2002 and 2013/2014 in Dronning Maud Land. As a previous study found increasing organochlorine concentrations with sampling day during the 2001/2002 breeding season, suggesting dietary changes, we investigated if this increase was repeated in the 2013/2014 breeding season. In addition to organochlorines, we analyzed hydroxy-metabolites, brominated contaminants and per- and polyfluoroalkyl substances (PFAS) in 2013/2014, as well as dietary descriptors of stable isotopes of carbon and nitrogen, to assess potential changes in diet during breeding. Lipid normalized concentrations of individual OHCs were 63%, 87% and 105% higher for hexachlorobenzene (HCB), 1,1-dichloro-2,2-bis (p-chlorophenyl)ethylene (p,p'-DDE), and ∑Polychlorinated biphenyls (PCBs), respectively, in 2013/2014 compared to 2001/2002. South polar skuas males in 2013/2014 were in poorer body condition than in 2001/2002, and with higher pollutant levels. Poorer body condition may cause the remobilization of contaminants from stored body reserves, and continued exposure to legacy contaminants at overwintering areas may explain the unexpected higher OHC concentrations in 2013/2014 than 2001/2002. Concentrations of protein-associated PFAS increased with sampling day during the 2013/2014 breeding season, whereas the lipid-soluble chlorinated pesticides, PCBs and polybrominated diphenyl ether (PBDEs) showed no change. OHC occurrence was not correlated with stable isotopes. The PFAS biomagnification through the local food web at the colony should be investigated further.
Show more [+] Less [-]Seabird breeding islands as sinks for marine plastic debris
2021
Grant, Megan L. | Lavers, Jennifer L. | Hutton, Ian | Bond, Alexander L.
Seabirds are apex predators in the marine environment and well-known ecosystem engineers, capable of changing their terrestrial habitats by introducing marine-derived nutrients via deposition of guano and other allochthonous inputs. However, with the health of the world’s oceans under threat due to anthropogenic pressures such as organic, inorganic, and physical pollutants, seabirds are depositing these same pollutants wherever they come to land. Using data from 2018 to 2020, we quantify how the Flesh-footed Shearwater (Ardenna carneipes) has inadvertently introduced physical pollutants to their colonies on Lord Howe Island, a UNESCO World Heritage site in the Tasman Sea and their largest breeding colony, through a mix of regurgitated pellet (bolus) deposition and carcasses containing plastic debris. The density of plastics within the shearwater colonies ranged between 1.32 and 3.66 pieces/m² (mean ± SE: 2.18 ± 0.32), and a total of 688,480 (95% CI: 582,409–800,877) pieces are deposited on the island each year. Our research demonstrates that seabirds are a transfer mechanism for marine-derived plastics, reintroducing items back into the terrestrial environment, thus making seabird colonies a sink for plastic debris. This phenomenon is likely occurring in seabird colonies across the globe and will increase in severity as global plastic production and marine plastic pollution accelerates without adequate mitigation strategies.
Show more [+] Less [-]Persistent pollutants in Northern Gannet Morus bassanus eggs in Ireland: Levels and colony differences
2021
Power, Andrew | White, Philip | McHugh, Brendan | Berrow, Simon | Schlingermann, Moira | Tannian, Marissa | Newton, Stephen | McGovern, E. (Evin) | Murphy, Sinéad | Crowley, Denis | O’Hea, Linda | Boyle, Brian | O’Connor, Ian
Seabird eggs are considered a favourable matrix for monitoring marine pollutants and are widely used as higher trophic level indicators. Persistent organic pollutants such as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and other organochlorine compounds (OCs) as well as metals have been shown to have deleterious impacts on seabirds. The Northern Gannet Morus bassanus is an avian sentinel; the largest breeding seabird in Ireland and an obligate piscivore. Gannet eggs were collected from two island colonies off the east coast of Ireland in locations with divergent history of industrialisation. Contaminant levels were measured and differences in concentrations between colonies compared. Stable isotope ratios of carbon (δ₁₃C) and nitrogen (δ₁₅N) were measured in each egg to understand the influence of diet and trophic position on contaminant levels detected. Significantly higher levels of Σ14PCBs, Σ7PBDEs and total mercury were detected in Gannet eggs from Lambay Island near Dublin (Ireland’s industrialised capital city) compared to Great Saltee Island. No differences were observed in levels of other OCs (HCB, ΣHCH, ΣCHL, ΣDDT) between the two colonies. Though Gannets travel significant distances when foraging for food, tracking studies have demonstrated that birds from proximal breeding colonies maintain exclusive feeding areas. Stable isotope ratio analysis in this study demonstrated that Gannets at both locations occupy similar dietary niches, indicating that dietary differences may not be the driver of differing contaminant levels between colonies. Levels of persistent pollutants in the Gannet eggs fall below most existing thresholds for adverse effects and are within internationally reported values. Recent population growth and range expansion of Gannets in Ireland suggest that persistent pollutants are not having an immediate impact on the Gannet population. This study will inform potential monitoring programmes that can help Ireland achieve good environmental status under the European Union’s Marine Strategy Framework Directive.
Show more [+] Less [-]Soil eutrophication in seabird colonies affects cell wall composition: Implications for the conservation of rare plant species
2021
Otero, X.L. | Fernández-Balado, C. | Ferreira, T.O. | Pérez-Alberti, A. | Revilla, G.
Seabird colonies exert a strong influence on coastal ecosystems, increasing soil nitrogen bioavailability and modifying plant communities. Previous studies have evidenced that increased N in soils leads to changes in plant cell wall composition; however, this effect has not been assessed in seabird colonies. The main objective of this study was to determine the influence of seabird colonies on nitrogen, cellulose and lignin content in cell walls. For this purpose, analyses were performed on droppings, soils and three native plant species (Armeria pubigera, Armeria pungens and Corema album) growing in yellow-legged gull colonies. The results showed that N excreted by yellow-legged gull is assimilated by plants, increases N content in plant tissues and reduces cellulose and lignin synthesis, therefore potentially altering plant resistance against phytoparasites.
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