Bird embryos perceive vibratory cues of predation risk from clutch mates

Noguera, J.C. and Velando, A., 2019. Bird embryos perceive vibratory cues of predation risk from clutch mates. Nature ecology & evolution, 3(8), pp.1225-1232.

During development in fluctuating environments, phenotypes can be adjusted to the conditions that individuals will probably encounter later in life. As developing embryos have a limited capacity to fully capture environmental information, theory predicts that they should integrate relevant information from all reliable sources, including the social environment. In many oviparous species, embryos are able to perceive cues of predator presence in some circumstances, but whether this information is socially transmitted among clutch mates—promoting phenotypic adjustments in the whole clutch—is unknown. Here, using an experimental design for which we modified the exposure to some, but not all, embryos of the same clutch to cues of predator presence (that is, alarm calls), we show that exposed embryos of the yellow-legged gull (Larus michahellis) and their unexposed clutch mates showed similar developmental changes that were absent in embryos from control clutches. Compared with the control broods, both embryos that were exposed to alarm calls and their unexposed clutch mates showed altered prenatal and postnatal behaviours, higher levels of DNA methylation and stress hormones, and reduced growth and numbers of mitochondria (which may be indicative of the capacity for energy production of cells). These results strongly suggest that gull embryos are able to acquire relevant environmental information from their siblings. Together, our results highlight the importance of socially acquired information during the prenatal stage as a non-genetic mechanism promoting developmental plasticity.

Marine megafauna niche coexistence and hotspot areas in a temperate ecosystem

Louzao, M., Valeiras, J., García-Barcelona, S., González-Quirós, R., Nogueira, E., Iglesias, M., Bode, A., Vázquez, J.A., Murcia, J.L., Saavedra, C. and Pierce, G.J., 2019. Marine megafauna niche coexistence and hotspot areas in a temperate ecosystem. Continental Shelf Research, 186, pp.77-87. 

In the last few decades, there has been a remarkable development of niche models to help understand the ecological response of species to current rapid environmental changes. In the present study, we applied niche modelling to the megafauna community of shelf waters of the northwestern (NW) and northern Iberian Peninsula in order to analyse the coexistence of different species taking into consideration their niche preferences. The Spanish Institute of Oceanography conducts the PELACUS multidisciplinary survey annually to assess pelagic fish stocks and collect information on the status of other ecosystem components, such as oceanographic conditions, phytoplankton, zooplankton and marine megafauna. Using data collected from these surveys, we developed niche models for 14 marine megafauna taxa (3 cetaceans, 10 seabirds and 1 fish) incorporating multi-trophic ecological descriptors collected simultaneously during the surveys alongside the more commonly used oceanographic variables (e.g. chlorophyll a and sea surface temperature). Megafauna niche models were developed by pooling observations from 2007 to 2013 and were found to be driven by mean fish biomass and its variability, in addition to sea surface temperature. Hierarchical clustering identified four distinct megafauna assemblages, the first comprising wide-ranging species and the other three associated with shelf-slope waters in Galicia, coastal/shelf waters in Galicia, and the eastern Cantabrian Sea, respectively. Community-level hotspot areas were found in shelf and shelf-break sectors of Galicia, along with small diversity spots scattered throughout the Cantabrian coastal area. Our results showed that synoptically collected survey-based ecological descriptors, especially acoustic-based preyscapes, were among the most important variables explaining megafauna niche preference. These findings highlight the advantage of using integrated ecosystem surveys to collect simultaneous information on a suite of ecosystem components for spatial assessments.


Metal content in the liver, kidney, and feathers of Northern gannets, Morus bassanus, sampled on the Spanish coast

The value of birds as bioindicators for monitoring the environmental inorganic elements has been globally recognized. In this context, due to its well-known ecology and population stability, the Northern gannet (Morus bassanus) could be particularly useful. Dead Northern gannets (n = 30) were collected and samples from the liver, kidney, and feathers were taken, dried, mineralized, and finally analyzed via ICP-MS. Metals and metalloids, namely As, Cd, Hg, Pb, and Zn, associated with environmental pollution and toxicity on living organisms, were evaluated. The mean highest concentrations of As, Hg, and Zn were found in the liver (0.916, 7.026, and 89.81 mg/kg dry weight, respectively). For Cd, the kidney showed the highest mean concentration (17.51 mg/kg dry weight), whereas for Pb, this value corresponded to the feathers (0.399 mg/kg dry weight). Significant differences were found between the age classes in terms of contaminant concentrations, with the adults exhibiting higher metal levels. This difference was significantly relevant for Pb and Hg, where the effect of age was observed for all the considered tissues. When considering the effect of gender, no significant differences were observed, in agreement with similar studies performed in other geographical regions. Finally, positive correlations between the concentrations of Hg and Pb in the feathers and in the liver (r = 0.688, p < 0.001 and r = 0.566, p < 0.001, respectively) were observed, as well as between the feather and kidney concentrations (r = 0.685, p < 0.001) indicating the possibility to use feathers, a non-invasive biomonitoring tissue, for better understanding Hg and Pb exposure in seabirds.

Lead (Pb) in the tissues of Anatidae, Ardeidae, Sternidae and Laridae of the Northern Hemisphere: a review of environmental studies

Korbecki, J., Gutowska, I., Chlubek, D. and Baranowska-Bosiacka, I., 2019. Lead (Pb) in the tissues of Anatidae, Ardeidae, Sternidae and Laridae of the Northern Hemisphere: a review of environmental studies. Environmental Science and Pollution Research, 26(13), pp.12631-12647.

Due to the ability of birds to travel long distances in the air, the potential feeding area of each individual is much larger than that of typical terrestrial animals. This makes birds a convenient indicator of environmental lead (Pb) pollution over large areas, in particular areas of inland and coastal waters. The aim of this study was to assess the concentrations of Pb in various organs of water birds from a variety of locations. The focus was on ducks, geese and swans (Anatidae); herons and egrets (Ardeidae); terns (Sternidae); and gulls (Laridae). This article describes the level of lead in the most commonly studied tissue types: feathers, bones and the liver. The study also presents data concerning the concentration of lead in the eggs of water birds. The highest levels of lead pollution can be observed in China and Korea, related to their high level of industrialization. In Iran too, environmental lead pollution is high, likely due to the developed petrochemical industry. Lead pollution in Japan, as well as in Western European countries (Spain, France, Italy), seems to be much lower than in China, India or Iran. Nevertheless, the level of pollution in Europe is higher than satisfactory, despite the introduction of a number of bans related to, for example, the use of leaded petrol or lead-containing paints. Finally, the USA and Canada appear to be the areas with the lowest lead pollution, possibly due to their low population densities.

Redox-regulation and life-history trade-offs: scavenging mitochondrial ROS improves growth in a wild bird

Velando, A., Noguera, J.C., da Silva, A. e Kim, S.Y., 2019. Redox-regulation and life-history trade-offs: scavenging mitochondrial ROS improves growth in a wild bird. Scientific reports, 9(1), p.2203.

It has been proposed that animals usually restrain their growth because fast growth leads to an increased production of mitochondrial reactive oxygen species (mtROS), which can damage mitochondrial DNA and promote mitochondrial dysfunction. Here, we explicitly test whether this occurs in a wild bird by supplementing chicks with a mitochondria-targeted ROS scavenger, mitoubiquinone (mitoQ), and examining growth rates and mtDNA damage. In the yellow-legged gull Larus michahellis, mitoQ supplementation increased the early growth rate of chicks but did not reduce mtDNA damage. The level of mtDNA damage was negatively correlated with chick mass, but this relationship was not affected by the mitoQ treatment. We also found that chick growth was positively correlated with both mtDNA copy number and the mitochondrial enzymatic activity of citrate synthase, suggesting a link between mitochondrial content and growth. Additionally, we found that mitoQ supplementation increased mitochondrial content (in males), altered the relationship between mtDNA copy number and damage, and downregulated some transcriptional pathways related to cell rejuvenation, suggesting that scavenging mtROS during development enhanced growth rates but at the expense of cellular turnover. Our study confirms the central role of mitochondria modulating life-history trade-offs during development by other mechanisms than mtROS-inflicted damage.


The use of European shag pellets as indicators of microplastic fibers in the marine environment

Álvarez, G., Barros, Á. and Velando, A., 2018. The use of European shag pellets as indicators of microplastic fibers in the marine environment. Marine Pollution Bulletin, 137, pp.444-448.

Microplastic particles are abundant marine pollutants that are ingested by many seabirds. Some seabirds regurgitate non-digestible materials in the form of pellets and their analysis may be useful to study the abundance of plastic debris at the local scale. Here, we aimed to provide baseline data for the presence of microplastics in pellets regurgitated by European shags (Phalacrocorax aristotelis) (n = 41) in the Iberia peninsula (NW Spain). We found microplastic fibers in 63% of pellets, suggesting that this type of plastic pollution is prevalent in the study area. According to Fourier Transform Infrared spectrometry, nylon fibers were the most abundant, followed by polyester. We also found that the presence of microplastics was higher in pellets containing remains of benthic fishes. Our results suggest that shag pellets may be useful to monitor microplastic pollution in coastal waters.

Concentrations of chlorinated pollutants in adipose tissue of yellow-legged gulls (Larus michahellis) from Spain: Role of gender and age

Vizuete, J., Hernández-Moreno, D., Fidalgo, L.E., Bertini, S., Andreini, R., Soler, F., Míguez-Santiyán, M.P., López-Beceiro, A. e Pérez-López, M., 2018. Concentrations of chlorinated pollutants in adipose tissue of yellow-legged gulls (Larus michahellis) from Spain: Role of gender and age. Ecotoxicology and environmental safety, 164, pp.493-499.

Concentrations of 7 different polychlorinated biphenyl (PCB) congeners, and eleven organochlorine pesticides (OCPs) and metabolites, including DDTs (dichlorodiphenyltrichloroethane), HCHs (hexachlorocyclohexane isomers), Endosulfan, Endosulfan sulfate, Endrin, Dieldrin and HCB (hexachlorobenzene), were determined in adipose tissue of 57 yellow-legged gulls collected from NW and N Spain. Furthermore, the possible differences due to two endogenous factors, age and gender, were determined. All the analyzed PCBs were detected in over 66% of the samples, with levels of 291.9 (PCB 180), 34.5 (PCB 118), 0.7 (PCB 28), 432.6 (PCB 153), 225.5 (PCB 138), 1.3 (PCB 101) and 0.4 (PCB 52) µg/kg of adipose tissue. With respect to the OCPs and metabolites, only 4,4′-DDE and HCB were detected in more than 50% of the samples, with means of 360.6 and 2.5 µg/kg of adipose tissue, respectively. From all the considered contaminants, only 4,4′-DDE levels presented significant differences depending on the gender, with females showing higher values than males (p < 0.01). Significant differences (p < 0.001) were also found related to age for the levels of PCBs 180, 138, 101, 28 and 153, as well as 4,4′-DDE, with adult levels being higher than those in young birds. The results of the present study constitute a baseline to better assess the environmental impacts of PCB and OCP contamination at other coastal sites for future biomonitoring studies, with particular emphasis on gender- and age-related differences.

Enrichment of trace elements in colonies of the yellow-legged gull (Larus michahellis) in the Atlantic Islands National Park (Galicia-NW Spain)

De La Peña-Lastra, S., Pérez-Alberti, A. e Otero, X.L., 2019. Enrichment of trace elements in colonies of the yellow-legged gull (Larus michahellis) in the Atlantic Islands National Park (Galicia-NW Spain). Science of The Total Environment, 648, pp.1536-1548.

Marine-derived nutrients are known accumulate in seabird breeding colonies due to the deposition of nutrient-rich biological materials, thus greatly altering the functioning and dynamics of these terrestrial ecosystems. Here we present the results of a sampling survey carried out during three years in yellow-legged gull colonies in the Atlantic Islands of Galicia National Park (NW Spain) with the aim of evaluating the influence of the colonies on the accumulation of trace elements, including micronutrients (Cu, Zn, Se, Co, Mo, Ni) and toxic elements (Cr, Cd, Hg, Pb, As, Ag), in the surrounding environments. For this purpose, we analysed samples of biological materials produced by the seabirds (pellets, excrement, feathers, eggs) and of soil, plants and inland water from several different subcolonies and control zones without seabirds.

The concentrations of most of the elements were higher in excrement and pellets (mean values: Zn: 152, As: 50 mg kg−1, Cd: 6, Co: 5 mg kg−1) than in feathers and eggs. The flow of trace elements into the breeding colonies, considering only the excrement, revealed a very high level of trace element deposition for a supposedly pristine environment (Zn: 2667, Cd: 70, Cu: 315, As: 64 g ha−1). The total concentrations of trace elements in soil were consistent with the long-term impact of the seabirds. Thus, the values in areas which this impact was greatest were significantly higher than in the control zones, particularly considering the most labile geochemical fractions of the soil. The concentrations of some elements (i.e. Co, As, Cd) were also higher in the inland waters in the colonies than in control zones. Finally, the concentration of trace elements in plants varied depending on the species and element considered.

Trace elements in biomaterials and soils from a Yellow-legged gull (Larus michahellis) colony in the Atlantic Islands of Galicia National Park (NW Spain).


Otero, X.L., de la Peña-Lastra, S., Romero, D., Nobrega, G.N., Ferreira, T.O., Pérez-Alberti, A., 2018. Trace elements in biomaterials and soils from a Yellow-legged gull (Larus michahellis) colony in the Atlantic Islands of Galicia National Park (NW Spain). Marine Pollution Bulletin, 133, pp.144-149.

Seabird colonies drastically transform the sites that they inhabit. Although the influence of seabirds on nutrient cycling has been investigated in numerous studies, the effects on trace elements has scarcely been considered. In this study, we determined the total contents of 9 trace elements in biomaterials (excrement, pellets, feathers and eggs) and soils in relation to the presence the Yellow-legged gull Larus michahellis. The concentrations of Zn, Cu and As were particularly high in the pellets and excrement. The total contents of the trace elements were significantly higher in the soils in the sub-colonies in which Yellow-legged gulls predominate than in soil from the control zone (with no gulls). The difference was even higher for the most reactive geochemical fractions. We observed that the oxidizable fraction was the most relevant fraction for almost all trace elements, indicating the importance of organic matter in trace element retention in sandy soils.

Presence and impact of Stockholm Convention POPs in gull eggs from Spanish and Portuguese natural and National Parks

Zapata, P., Ballesteros-Cano, R., Colomer, P., Bertolero, A., Viana, P., Lacorte, S., Santos, F.J., 2018. Presence and impact of Stockholm Convention POPs in gull eggs from Spanish and Portuguese natural and national parks. Science of The Total Environment, 633, pp.704-715.

The aim of the present work was to comparatively assess the occurrence and impact of persistent organic pollutants (POPs) in nine natural and national parks from Spain and Portugal using gull eggs (Larus michahellis and L. audouinii) as bioindicators of environmental contamination. Sampling was performed during the breeding season of 2016. Compounds studied include polychlorinated biphenyls (PCBs), organochlorinated pesticides (OC pesticides), perfluorooctane sulfonic acid (PFOS) and polybrominated diphenyl ethers (PBDEs), and were analyzed using mass spectrometric based techniques. The results showed a high contamination by PCBs in all colonies, with total levels ranging from 59 to 1278 ng/g wet weight (ww), despite their use is not currently authorized. OC pesticides were also present in all colonies, with a high incidence of 4,4′-DDE in gull eggs at levels up to 218 ± 50 ng/g ww in L. michahellis and 760 ± 412 ng/g ww in L. audouinii from the Ebro Delta natural park. PBDEs and PFOS were also detected at levels up to 91.7 ± 21.3 ng/g ww, which can be attributed to a more recent use. Except for PBDEs, the POP levels in eggs from L. audouinii were higher than in L. michahellis, presumably associated to the fish-based diet of the former. Finally, the effect of POP levels on eggshell parameters (volume, eggshell thickness and desiccation index) were investigated for each colony and gull species in order to evaluate the egg viability and, therefore, the reproduction success.