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Blood mercury concentrations in four sympatric gull species from South Western France: Insights from stable isotopes and biologging
2022
Jouanneau, William | Sebastiano, Manrico | Rozen-Rechels, David | Harris, Stephanie M. | Blévin, Pierre | Angelier, Frédéric | Brischoux, François | Gernigon, Julien | Lemesle, Jean-Christophe | Robin, Frédéric | Cherel, Yves | Bustamante, Paco | Chastel, Olivier
Mercury (Hg) is a toxic trace element widely distributed in the environment, which particularly accumulates in top predators, including seabirds. Among seabirds, large gulls (Larus sp) are generalist feeders, foraging in both terrestrial and marine habitats, making them relevant bioindicators of local coastal Hg contamination. In the present study, we reported blood Hg concentrations in adults and chicks of four different gull species breeding on the French Atlantic coast: the European herring gull (Larus argentatus), the Lesser black-backed gull (L. fuscus), the Great black-backed gull (L. marinus) and the Yellow-legged gull (L. michahellis). We also investigated the potential role of foraging ecology in shaping Hg contamination across species, using the unique combination of three dietary tracers (carbon, nitrogen and sulfur stable isotopes) and biologging (GPS tracking). A high concentration of Hg was associated with high trophic position and a marine diet in gulls, which was corroborated by birds’ space use strategy during foraging trips. Adults of all four species reached Hg concentrations above reported toxicity thresholds. Specifically, adults of Great black-backed gulls had a high trophic marine specialized diet and significantly higher Hg concentrations than the three other species. Blood Hg was 4–7 times higher in adults than in chicks, although chicks of all species received mainly marine and high trophic position prey, which is expected to be the cause of blood Hg concentrations of toxic concern. By using both stable isotopes and GPS tracking, the present study provides compelling insights on the main feeding habits driving Hg contamination in a seabird assemblage feeding in complex coastal environments.
Show more [+] Less [-]Mercury biomagnification in an Antarctic food web of the Antarctic Peninsula
2022
Matias, Ricardo S. | Guímaro, Hugo R. | Bustamante, Paco | Seco, José | Chipev, N. | Fragão, Joana | Tavares, Sílvia | Ceia, Filipe R. | Pereira, Maria E. | Barbosa, Andrés | Xavier, José C.
Under the climate change context, warming Southern Ocean waters may allow mercury (Hg) to become more bioavailable to the Antarctic marine food web (i.e., ice-stored Hg release and higher methylation rates by microorganisms), whose biomagnification processes are poorly documented. Biomagnification of Hg in the food web of the Antarctic Peninsula, one of the world's fastest-warming regions, was examined using carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotope ratios for estimating feeding habitat and trophic levels, respectively. The stable isotope signatures and total Hg (T-Hg) concentrations were measured in Antarctic krill Euphausia superba and several Antarctic predator species, including seabirds (gentoo penguins Pygoscelis papua, chinstrap penguins Pygoscelis antarcticus, brown skuas Stercorarius antarcticus, kelp gulls Larus dominicanus, southern giant petrels Macronectes giganteus) and marine mammals (southern elephant seals Mirounga leonina). Significant differences in δ¹³C values among species were noted with a great overlap between seabird species and M. leonina. As expected, significant differences in δ¹⁵N values among species were found due to interspecific variations in diet-related to their trophic position within the marine food web. The lowest Hg concentrations were registered in E. superba (0.007 ± 0.008 μg g⁻¹) and the highest values in M. giganteus (12.090 ± 14.177 μg g⁻¹). Additionally, a significant positive relationship was found between Hg concentrations and trophic levels (reflected by δ¹⁵N values), biomagnifying nearly 2 times its concentrations at each level. Our results support that trophic interaction is the major pathway for Hg biomagnification in Southern Ocean ecosystems and warn about an increase in the effects of Hg on long–lived (and high trophic level) Antarctic predators under climate change in the future.
Show more [+] Less [-]Towards a North Pacific Ocean long-term monitoring program for plastic pollution: A review and recommendations for plastic ingestion bioindicators
2022
Savoca, Matthew S. | Kuhn, Susanne | Sun, ChengJun | Avery-Gomm, Stephanie | Choy, C Anela | Dudas, Sarah | Hong, Sang Hee | Hyrenbach, K David | Li, Zongxian | Ng, Connie Ka-yan | Provencher, Jennifer F. | Lynch, Jennifer M.
Marine debris is now a ubiquitous component of the Anthropocene global ocean. Plastic ingestion by marine wildlife was first reported in the 1960s and since that time, roughly one thousand marine species have been reported to consume this debris. This study focuses on plastic ingestion by marine invertebrates and vertebrates in the North Pacific Ocean. Specifically, we reviewed the scientific literature to assess the scope of the problem, identified key bioindicator species, and proposed guidelines for future monitoring of plastic debris in North Pacific marine ecosystems. Our meta-analysis confirmed that the North Pacific is among the most polluted ocean regions globally; roughly half of all fish and seabird specimens and more than three-quarters of sea turtles and bivalve specimens examined in this region had consumed plastic. While there are not enough standardized data to assess if these ingestion rates are changing, sampling standardization and reporting of methods are improving over time. Using a rubric-evaluation approach, we evaluated 352 species for their potential to serve as bioindicators of the prevalence of plastic pollution in the North Pacific. This analysis revealed a suite of 12 bioindicator species candidates which sample a variety of ecosystem components and cover a wide range of plastic size classes. Thus, we contend that these bioindicator candidates provide a key foundation for developing a comprehensive plastic monitoring program in the region. To enhance the utility of these bioindicators, we developed a framework for standardized data collection to minimize methodological variability across different studies and to facilitate the assessment of temporal trends over space and time. Tracking plastic ingestion by these bioindicators will help to assess the effectiveness of mitigation actions in the region, a critical step to evaluate progress towards sustainability and improved ocean health in the 21st century.
Show more [+] Less [-]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 [-]In vitro avian bioaccessibility of metals adsorbed to microplastic pellets
2020
Microplastics are known to be associated with co-contaminants, but little is understood about the mechanisms by which these chemicals are transferred from ingested plastic to organisms. This study simulates marine avian gastric conditions in vitro to examine the bioaccessibility of authigenic metals (Fe, Mn) and trace metals (Co, Pb) that have been acquired by polyethylene microplastic pellets from their environment. Specifically, different categories of pellet were collected from beaches in Cornwall, southwest England, and exposed to an acidified saline solution of pepsin (pH ∼ 2.5) at 40 °C over a period of 168 h with extracted metal and residual metal (available to dilute aqua regia) analysed by ICP-MS. For Fe, Mn and Co, kinetic profiles consisted of a relatively rapid initial period of mobilisation followed by a more gradual approach to quasi-equilibrium, with data defined by a diffusion model and median rate constants ranging from about 0.0002 (μg L⁻¹)⁻¹ h⁻¹ for Fe to about 7 (μg L⁻¹)⁻¹ h⁻¹ for Co. Mobilisation of Pb was more complex, with evidence of secondary maxima and re-adsorption of the metal to the progressively modified pellet surface. At the end of the time-courses, maximum total concentrations were 38.9, 0.81, 0.014 and 0.10 μg g⁻¹ for Fe, Mn, Co and Pb, respectively, with maximum respective percentage bioaccessibilities of around 60, 80, 50 and 80. When compared with toxicity reference values for seabirds, the significance of metals acquired by microplastics from the environment and exposed to avian digestive conditions is deemed to be low, but studies of a wider range of plastics and metal associations (e.g. as additives) are required for a more comprehensive risk assessment.
Show more [+] Less [-]Confidence intervals and sample size for estimating the prevalence of plastic debris in seabird nests
2020
Evidence is accumulating about the impacts of plastics on marine life. The prevalence of plastics in seabird nests has been used as an indicator of levels of this pollutant in the ocean. However, the lack of a framework for defining sample sizes and errors associated with estimating the prevalence of plastic in nests prevents researchers from optimising time and reducing impacts of fieldwork. We present a method to determine the confidence intervals for the prevalence of debris in seabird nests and provide, for the first time, information on the prevalence of these items in nests of the Hartlaub’s gull Larus hartlaubii, the African penguin Spheniscus demersus, the great white pelican Pelecanus onocrotalus, and the white-breasted cormorant Phalacrocorax lucidus in South Africa. The method, based on observations and resampling simulations and tested here for nests of 12 seabird species from 15 locations worldwide, allows for straightforward hypothesis testing. Appropriate sample sizes can be defined by combining this method with a Bayesian approach. We show that precise estimates of prevalence of debris in nests can be obtained by sampling around 250 nests. Smaller sample sizes can be useful for obtaining rough estimates. For the Hartlaub’s gull, the African penguin, the great white pelican, and the white-breasted cormorant, debris were present in 0.75%, 3.00%, 6.41%, and 25.62% of the respective nests. Our approach will help researchers to determine errors associated with the prevalence of debris recorded in seabird nests and to optimise time and costs spent collecting data. It can also be applied to estimate confidence intervals and define sample sizes for assessing prevalence of plastic ingestion by any organism.
Show more [+] Less [-]Seabird plastic ingestion differs among collection methods: Examples from the short-tailed shearwater
2018
Rodríguez, Airam | Ramirez, Francisco | Carrasco, M Nazaret | Chiaradia, André
Despite the increase of literature on seabird plastic ingestion in recent years, few studies have assessed how plastic loads vary according to different sampling methods. Most studies use necropsies of seabirds with a natural cause of death, e.g. beached or predated, to determine plastic loads and monitor marine debris. Sampling naturally dead seabirds may be biased as they have perished because of their intrinsic factors, e.g. poor body condition, high parasite loads, sickness or predation, affecting estimates of plastic loads. However, seabirds killed accidentally may be more representative of the population. Here, we used the short-tailed shearwater Ardenna tenuirostris to test different sampling methods: naturally beached fledglings and accidentally road-killed fledglings after being attracted and grounded by artificial lights. We compared plastic load, body condition, and feeding strategies (through using feathers’ δ¹³C and δ¹⁵N isotope niche) between beached and road-killed fledglings. Beached birds showed higher plastic loads, poorer body condition and reduced isotopic variability, suggesting that this group is not a representative subsample of the whole cohort of the fledgling population. Our results might have implications for long-term monitoring programs of seabird plastic ingestion. Monitoring plastic debris through beached birds could overestimate plastic ingestion by the entire population. We encourage the establishment of refined monitoring programs using fledglings grounded by light pollution if available. These samples focus on known cohorts from the same population. The fledgling plastic loads are transferred from parents during parental feeding, accumulating during the chick-rearing period. Thus, these fledglings provide a higher and valuable temporal resolution, which is more useful and informative than unknown life history of beached birds.
Show more [+] Less [-]Accumulate or eliminate? Seasonal mercury dynamics in albatrosses, the most contaminated family of birds
2018
Cherel, Yves | Barbraud, Christophe | Lahournat, Maxime | Jaeger, Audrey | Jaquemet, Sébastien | Wanless, Ross M. | Phillips, Richard A. | Thompson, D. R. (David R.) | Bustamante, Paco
Albatrosses (Diomedeidae) are iconic pelagic seabirds whose life-history traits (longevity, high trophic position) put them at risk of high levels of exposure to methylmercury (MeHg), a powerful neurotoxin that threatens humans and wildlife. Here, we report total Hg (THg) concentrations in body feathers from 516 individual albatrosses from 35 populations, including all 20 taxa breeding in the Southern Ocean. Our key finding is that albatrosses constitute the family of birds with the highest levels of contamination by Hg, with mean feather THg concentrations in different populations ranging from moderate (3.8 μg/g) to exceptionally high (34.6 μg/g). Phylogeny had a significant effect on feather THg concentrations, with the mean decreasing in the order Diomedea > Phoebetria > Thalassarche. Unexpectedly, moulting habitats (reflected in feather δ13C values) was the main driver of feather THg concentrations, indicating increasing MeHg exposure with decreasing latitude, from Antarctic to subtropical waters. The role of moulting habitat suggests that the majority of MeHg eliminated into feathers by albatrosses is from recent food intake (income strategy). They thus differ from species that depurate MeHg into feathers that has been accumulated in internal tissues between two successive moults (capital strategy). Since albatrosses are amongst the most threatened families of birds, it is noteworthy that two albatrosses listed as Critical by the World Conservation Union (IUCN) that moult and breed in temperate waters are the most Hg-contaminated species (the Amsterdam and Tristan albatrosses). These data emphasize the urgent need for robust assessment of the impact of Hg contamination on the biology of albatrosses and they document the high MeHg level exposure of wildlife living in the most remote marine areas on Earth.
Show more [+] Less [-]Perfluorinated substances and telomeres in an Arctic seabird: Cross-sectional and longitudinal approaches
2017
Blévin, Pierre | Angelier, Frédéric | Tartu, Sabrina | Bustamante, Paco | Herzke, Dorte | Moe, Børge | Bech, Claus | Gabrielsen, Geir Wing | Bustnes, Jan Ove | Chastel, Olivier
Telomeres are non-coding DNA repeats located at the termini of eukaryotic chromosomes, regulated by dynamic processes balancing shortening and maintenance. Despite a mechanism to slow-down telomere shortening, cell division leads to progressive attrition of chromosomes, leading to the onset of cellular senescence or apoptosis. However, telomere restoration based on telomerase activity is the primary mechanism for telomere maintenance. Telomere length is associated to health and survival and can be impacted by a broad panel of environmental factors. However, the effect of contaminants on telomeres is poorly known for living organisms. The aim of this study was to investigate relationships between some poly- and perfluoroalkyl substances (PFASs), body condition and telomere length by using both a cross-sectional and longitudinal approach in adult breeding Black-legged kittiwakes (Rissa tridactyla) from Svalbard. First, we examined the associations between absolute telomere length and PFASs contamination in a given year (cross-sectional approach). Second, we investigated the relationships between telomere dynamics and PFASs contamination within a two years’ time frame (longitudinal approach). Our results did not show any significant relationships of PFASs and body condition with absolute telomere length in a given year. Surprisingly, we found a positive and significant relationship between PFASs and telomere dynamics in both sexes with elongated telomere in birds bearing the highest concentrations of PFASs. Our study underlines (i) the need to investigate PFAS effects on telomere dynamics with a longitudinal approach and (ii) a potential positive effect of these contaminants on telomere length, with the most contaminated birds showing the slowest rate of telomere shortening or even displaying elongated ones. Our study is the first to report a relationship between PFASs and telomere length in free-living vertebrates. A possible underlying mechanism and other potential confounding factors are discussed.
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