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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 [-]Regional variation in mercury bioaccumulation among NW Atlantic Golden (Lopholatilus chamaeleonticeps) and Blueline (Caulolatilus microps) Tilefish
2021
Roose, Hunter | Paterson, Gordon | Frisk, Michael G. | Cerrato, Robert M. | Nitschke, Paul | Olin, Jill A.
Mercury (Hg) concentrations in fishes from the NW Atlantic Ocean pose concern due to the importance of this region to U.S. fisheries harvest. In this study, total Hg (THg) concentrations and nitrogen stable isotope (δ¹⁵N) values were quantified in muscle tissues sampled from Golden (Lopholatilus chamaeleonticeps) and Blueline (Caulolatilus microps) Tilefish collected during a fishery-independent survey conducted in the NW Atlantic to compare bioaccumulation patterns between these species. Total Hg concentrations averaged (±SD) 0.4 ± 0.4 μg/g dry weight (d.w.) for L. chamaeleonticeps and 1.1 ± 0.7 μg/g d.w. for C. microps with <2% of all sampled fish, those >70 cm fork length, exceeding the most restrictive USEPA regulatory guidelines for human consumption (THg > 0.46 μg/g w.w.), when converted to wet weight concentrations. The THg concentrations reported here for individuals from the NW Atlantic stock are comparable to those reported for similarly sized individuals collected from the SW Atlantic stock but notably lower than those reported for Gulf of Mexico L. chamaeleonticeps, indicating different Hg exposure and assimilation kinetics for fish from the NW Atlantic, and highlights the broad geographic variability of Hg bioaccumulation among Tilefish stocks. Caulolatilus microps had higher δ¹⁵N values relative to L. chamaeleonticeps and a pattern of decreasing THg concentrations was also present from south to north across the study range. It is concluded that this trophic difference and spatial pattern in Tilefish THg concentrations emphasizes the habitat and resource partitioning mechanisms described for these sympatric species that permits their coexistence in the continental shelf environment. Importantly, regional variability in THg concentrations accentuate the possible roles of fine-scale biotic and abiotic processes that can act to regulate Hg bioaccumulation among individuals and species.
Show more [+] Less [-]Repeated conservation threats across the Americas: High levels of blood and bone lead in the Andean Condor widen the problem to a continental scale
2017
Wiemeyer, Guillermo M. | Perez, Miguel A. | Torres Bianchini, Laura | Sampietro, Luciano | Bravo, Guillermo F. | Jácome, N Luis | Astore, Vanesa | Lambertucci, Sergio A.
Wildlife lead exposure is an increasing conservation threat that is being widely investigated. However, for some areas of the world (e.g., South America) and certain species, research on this subject is still scarce or only local information is available. We analyzed the extent and intensity of lead exposure for a widely distributed threatened species, the Andean Condor (Vultur gryphus). We conducted the study at two different scales: 1) sampling of birds received for rehabilitation or necropsy in Argentina, and 2) bibliographic review and extensive survey considering exposure event for the species' distribution in South America. Wild condors from Argentina (n = 76) presented high lead levels consistent with both recent and previous exposure (up to 104 μg/dL blood level, mean 15.47 ± 21.21 μg/dL and up to 148.20 ppm bone level, mean 23.08 ± 31.39 ppm). In contrast, captive bred individuals -not exposed to lead contamination- had much lower lead levels (mean blood level 5.63 ± 3.08 μg/dL, and mean bone level 2.76 ± 3.06 ppm). Condors were exposed to lead throughout their entire range in continental Argentina, which represents almost sixty percent (>4000 km) of their geographical distribution. We also present evidence of lead exposure events in Chile, Ecuador, and Peru. Lead poisoning is a widespread major conservation threat for the Andean Condor, and probably other sympatric carnivores from South America. The high number and wide range of Andean Condors with lead values complement the results for the California Condor and other scavengers in North America suggesting lead poisoning is a continental threat. Urgent actions are needed to reduce this poison in the wild.
Show more [+] Less [-]Mercury isotopes as tracers of ecology and metabolism in two sympatric shark species
2020
Le Croizier, Gaël | Lorrain, Anne | Sonke, Jeroen E. | Jaquemet, Sébastien | Schaal, Gauthier | Renedo, Marina | Besnard, Lucien | Cherel, Yves | Point, David
In coastal ecosystems, top predators are exposed to a wide variety of nutrient and contaminant sources due to the diversity of trophic webs within inshore marine habitats. Mercury contamination could represent an additional threat to shark populations that are declining worldwide. Here we measured total mercury, carbon and nitrogen isotopes, as well as mercury isotopes, in two co-occurring shark species (the bull shark Carcharhinus leucas and the tiger shark Galeocerdo cuvier) and their potential prey from a coastal ecosystem of the western Indian Ocean (La Réunion Island). Our primary goals were to (i) determine the main trophic Hg sources for sharks and (ii) better characterize their diet composition and foraging habitat. Hg isotope signatures (Δ¹⁹⁹Hg and δ²⁰²Hg) of shark prey suggested that bull sharks were exposed to methylmercury (MeHg) produced in offshore epipelagic waters, while tiger sharks were exposed to offshore mesopelagic MeHg with additional microbial transformation in slope sediments. Δ¹⁹⁹Hg values efficiently traced the ecology of the two predators, demonstrating that bull sharks targeted coastal prey in shallow waters while tiger sharks were mainly foraging on mesopelagic species in the deeper waters of the island slope. Unexpectedly, we found a positive shift in δ²⁰²Hg (>1‰) between sharks and their prey, leading to high δ²⁰²Hg values in the two shark species (e.g. 1.91 ± 0.52‰ in bull sharks). This large shift in δ²⁰²Hg indicates that sharks may display strong MeHg demethylation abilities, possibly reflecting evolutionary pathways for mitigating their MeHg contamination.
Show more [+] Less [-]Interspecific variation of essential and non-essential trace elements in sympatric seabirds
2018
Moura, Jailson F. | Tavares, Davi C. | Lemos, Leila S. | Acevedo-Trejos, Esteban | Saint’Pierre, Tatiana Dillenburg | Siciliano, Salvatore | Merico, Agostino
Chemical pollution is a growing issue for ocean ecosystems, threatening especially apex predators because they bioaccumulate persistent chemical pollutants such as non-essential trace elements. The trophic position is thus a key aspect when assessing the impacts of environmental pollution in marine organisms. Here we investigate the differences in the concentrations of essential (Cu, Cr, Se, and Zn) and non-essential elements (Hg, Al, As, Cd, and Sr), in muscular and hepatic tissues of four sympatric non-migratory seabirds (namely Sula leucogaster, Larus dominicanus, Fregata magnificens, and Thalasseus acuflavidus), which were found stranded along the Brazilian coast. The observed hepatic and muscular interspecific differences in elemental concentrations indicated that these sympatric seabirds are differently exposed to persistent contaminants circulating in the food web due to differences with respect to known feeding behaviours and prey preferences. Moreover, we found a consistent co-accumulative relationship between Se and Hg molar levels in liver tissues with mean Se:Hg molar ratio above 1. This relationship supports previous studies indicating that Se, via the formation of SeHg complexes, plays an essential biochemical role in the detoxification process of methyl mercury in seabirds. Our results suggest that feeding behaviour is an important factor associated to the interspecific differences of trace element concentrations in seabirds. However, traits other than feeding preferences (e.g. age) may also play an important role in the accumulation of these elements.
Show more [+] Less [-]Blood concentrations of PCBs and DDTs in an avian predator endemic to southern Africa: Associations with habitat, electrical transformers and diet
2018
Garcia-Heras, Marie-Sophie | Arroyo, Beatriz | Simmons, Robert E. | Camarero, Pablo R. | Mateo, Rafael | Mougeot, Francois
Persistent pollutants such as organochlorine compounds (OCs) have been highlighted as a cause of population decline in avian predators. Understanding patterns of OCs contamination can be crucial for the conservation of affected species, yet little is known on these threats to African raptors. Here we report on OC concentrations in an endangered predator endemic to southern Africa, the Black Harrier Circus maurus. Blood samples were collected in 2012–2014 from wild nestlings (n = 90) and adults (n = 23) in south-western South Africa, where agriculture and urbanization have developed rapidly since the 1950s. Polychlorinated biphenyl (ΣPCB) and dichlorodiphenyltrichloroethane (ΣDDT, for p,p’-DDT + p,p’-DDE) were detected in 79% and 84% of sampled individuals, respectively, with varying concentrations among demographic groups: nestlings had significantly higher ΣPCB and p,p’-DDT concentrations than adults, while adults had higher levels of p,p’-DDE than nestlings. Levels of ΣPCB significantly increased with an index of electric transformer density, a measure of the number and power of electric transformers around active nests. We propose this index as a useful tool for assessing ΣPCB exposure risk in other wildlife. Levels of p,p’-DDE significantly increased with the proportion of wetlands within the breeding territory, and also with the proportion of bird biomass in the diet. No association was found between OC levels and the protected area status of nesting sites. Physiological effects of contaminants were also manifest in increased white blood cell counts with higher p,p’-DDT levels. Heterophil to lymphocyte ratio increased with higher ΣPCB levels, suggesting increased physiological stress and reduced immunity in contaminated individuals. Our results suggest that OCs are still a current cause of concern for endangered Black Harriers, as well as other sympatric predators.
Show more [+] Less [-]Anthropogenic noise alters dwarf mongoose responses to heterospecific alarm calls
2017
Morris-Drake, Amy | Bracken, Anna M. | Kern, Julie M. | Radford, Andrew N.
Anthropogenic noise is an evolutionarily novel and widespread pollutant in both terrestrial and aquatic habitats. Despite increasing evidence that the additional noise generated by human activities can affect vocal communication, the majority of research has focused on the use of conspecific acoustic information, especially sexual signals. Many animals are known to eavesdrop on the alarm calls produced by other species, enhancing their likelihood of avoiding predation, but how this use of heterospecific information is affected by anthropogenic noise has received little empirical attention. Here, we use two field-based playback experiments on a habituated wild population of dwarf mongooses (Helogale parvula) to determine how anthropogenic noise influences the response of foragers to heterospecific alarm calls. We begin by demonstrating that dwarf mongooses respond appropriately to the alarm calls of sympatric chacma baboons (Papio ursinus) and tree squirrels (Paraxerus cepapi); fleeing only to the latter. We then show that mongoose foragers are less likely to exhibit this flee response to tree squirrel alarm calls during road-noise playback compared to ambient-sound playback. One explanation for the change in response is that noise-induced distraction or stress result in maladaptive behaviour. However, further analysis revealed that road-noise playback results in increased vigilance and that mongooses showing the greatest vigilance increase are those that do not subsequently exhibit a flee response to the alarm call. These individuals may therefore be acting appropriately: if the greater gathering of personal information indicates the absence of an actual predator despite an alarm call, the need to undertake costly fleeing behaviour can be avoided. Either way, our study indicates the potential for anthropogenic noise to interfere with the use of acoustic information from other species, and suggests the importance of considering how heterospecific networks are affected by this global pollutant.
Show more [+] Less [-]Differing foraging strategies influence mercury (Hg) exposure in an Antarctic penguin community
2016
Polito, Michael J. | Brasso, Rebecka L. | Trivelpiece, Wayne Z. | Karnovsky, Nina | Patterson, William P. | Emslie, Steven D.
Seabirds are ideal model organisms to track mercury (Hg) through marine food webs as they are long-lived, broadly distributed, and are susceptible to biomagnification due to foraging at relatively high trophic levels. However, using these species as biomonitors requires a solid understanding of the degree of species, sexual and age-specific variation in foraging behaviors which act to mediate their dietary exposure to Hg. We combined stomach content analysis along with Hg and stable isotope analyses of blood, feathers and common prey items to help explain inter and intra-specific patterns of dietary Hg exposure across three sympatric Pygoscelis penguin species commonly used as biomonitors of Hg availability in the Antarctic marine ecosystem. We found that penguin tissue Hg concentrations differed across species, between adults and juveniles, but not between sexes. While all three penguins species diets were dominated by Antarctic krill (Euphausia superba) and to a lesser extent fish, stable isotope based proxies of relative trophic level and krill consumption could not by itself sufficiently explain the observed patterns of inter and intra-specific variation in Hg. However, integrating isotopic approaches with stomach content analysis allowed us to identify the relatively higher risk of Hg exposure for penguins foraging on mesopelagic prey relative to congeners targeting epipelagic or benthic prey species. When possible, future seabird biomonitoring studies should seek to combine isotopic approaches with other, independent measures of foraging behavior to better account for the confounding effects of inter and intra-specific variation on dietary Hg exposure.
Show more [+] Less [-]Environmental stress responses in sympatric congeneric crustaceans: Explaining and predicting the context-dependencies of invader impacts
2021
Ros, Macarena | Guerra-García, José M. | Lignot, Jehan-Hervé | Rivera-Ingraham, Georgina A.
The role of ecophysiology in mediating marine biological pollution is poorly known. Here we explore how physiological plasticity to environmental stress can explain and predict the context-dependencies of invasive species impacts. We use the case of two sympatric skeleton shrimps, the invader Caprella scaura and its congener C. equilibra, which is currently replaced by the former on the South European coast. We compare their physiological responses to hyposalinity stress under suboptimal low and high temperature, while inferring on hypoxia tolerance. We use an energy-redox approach, analyzing mortality rate, the energetic balance and the consequent effects on the oxidative homeostasis. We found that decreased seawater salinity and/or oxygen levels can weaken biotic resistance, especially in females of C. equilibra, leading to periods of heightened vulnerability to invasion. Our approach provides mechanistic insights towards understanding the factors promoting invader impacts, highlighting the potential of ecophysiology for improving invasive species management.
Show more [+] Less [-]Assessment of environmental health based on a complementary approach using metal quantification, oxidative stress and trophic ecology of two gull species (Larus michahellis &Larus audouinii) breeding in sympatry
2020
Laranjeiro, Maria I. | Alves, Luís M.F. | Silva, Joana M. | Calado, Joana G. | Norte, Ana C. | Paiva, Vítor H. | Lemos, Marco F.L. | Ramos, Jaime A. | Novais, Sara C. | Ceia, Filipe R.
Metal pollution is currently a major issue in marine ecosystems, as organisms, and particularly seabirds, are exposed and accumulating increased levels from several anthropogenic sources. A set of 13 metals were quantified in two gull species breeding in sympatry, and in two distinct colonies separated by ca. 400 km. Oxidative stress was measured, and stable isotope analyses were used to link metal contamination and oxidative stress with the trophic ecology of each species/population. There was a clear segregation of metal contamination between the two species and to a much lesser extent between colonies. Overall, Audouin's gull was the most contaminated species for most metals, once this species relies mainly on fish and other marine resources. The Yellow-legged gull feeds regularly on terrestrial food sources besides fish, which may dilute contamination levels. Oxidative stress responses were related with birds' trophic ecology and foraging habitat, but apparently not with metal contamination.
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