Variation in mercury concentration in juvenile ...

Environmental Pollution 238 (2018) 397e403

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Variation in mercury concentration in juvenile Magellanic penguins during their migration path along the Southwest Atlantic Ocean* ^ as Silveira c, Jailson F. Moura a, *, Davi C. Tavares a, Leila S. Lemos b, Victor Vilas-Bo Salvatore Siciliano c, Rachel A. Hauser-Davis d a

Leibniz Centre for Tropical Marine Research - ZMT, Bremen, Germany Department of Fisheries and Wildlife, Oregon State University, Newport, USA Instituto Oswaldo Cruz/Fiocruz, Rio de Janeiro, RJ, Brazil d ~o Oswaldo Cruz, Rio de Janeiro, Brazil Centro de Estudos da Saúde do Trabalhador e Ecologia Humana, Fundaça b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 23 June 2017 Received in revised form 8 March 2018 Accepted 8 March 2018 Available online 26 March 2018

The vulnerability of seabirds related to their migratory dynamics is frequently linked to environmental problems along the migration path. In this context, Magellanic penguins (Sphenicus magellanicus) seem to be vulnerable to an extensive range of environmental disturbances during their northward migration along the Atlantic waters of South America, which include by catch, marine debris ingestion, overfishing and environmental contamination. In this study, we investigate mercury accumulation in muscle and hepatic tissues of juveniles penguins collected along the Brazilian coast during three migratory seasonal years (2006, 2008 and 2012) and three areas along a latitudinal gradient. We found significant differences in Hg levels across the years, with higher hepatic Hg levels found in tissues of penguins sampled in 2008. The higher Hg levels in samples of penguins from 2008 might be attributed to variations in body ~ o event during condition or Hg uptake, associated with the trophic imbalance linked to an extreme El Nin that year. Significant differences in Hg accumulation across the latitudinal areas were also observed. The penguins sampled at the farthest area from the breeding ground presented the higher levels of Hg and also the poorest body condition. Body condition and other traits may influence the levels of chemical pollutants and decrease the migratory success rate in the juvenile age phase, compromising population dynamics. © 2018 Published by Elsevier Ltd.

Keywords: Spheniscus magellanicus Mercury Migration Brazil

1. Introduction Migratory species naturally face many survivorship challenges during their journeys in the marine environment, but ecological vulnerabilities have been aggravated due to human perturbations along the migration routes (Walther et al., 2002; Warner, 2010). Ecosystem disturbances, such as habitat loss and fragmentation and environmental pollution, pose a risk to the animals during their migration and can affect the viability of the population (Dolman and Sutherland, 1992; Robinson et al., 2009; Montevecchi et al., 2012; Tartu et al., 2013; Fort et al., 2015; Carravieri et al., 2017). Many seabirds, including penguins, are iconic species

*

This paper has been recommended for acceptance by Prof. W. Wen-Xiong. * Corresponding author. System Ecology Group, Leibniz Centre for Tropical Marine Research - ZMT, Bremen, Germany. E-mail address: [email protected] (J.F. Moura). https://doi.org/10.1016/j.envpol.2018.03.021 0269-7491/© 2018 Published by Elsevier Ltd.

specialized in long migrations, entailing considerable energetic costs with the locomotion, predation avoidance, search for suitable habitats and availability of prey, but also facing human-related population disturbances (Pütz et al., 2007; Quillfeldt et al., 2010; ron and Gre millet, 2013). Pe Every year, juvenile Magellanic penguins (Spheniscus magellanicus) perform a massive northward wintering migration along the Atlantic waters of South America from their breeding grounds, located on the coasts of southern Argentina, Chile and Falkland/ Malvinas Islands (García-Borboroglu et al., 2006; Pütz et al., 2007; Boersma et al., 2013). The northern extension of the wintering nonbreeding penguins distribution includes south and southeastern Brazil, although the northward limit of the wintering dispersion seems to be considerably expanded during the last decades (Dantas et al., 2013). In the previous years, this species has been regularly recorded along the Rio de Janeiro (22 580 S) coast, as well as on the coast, northeastern Brazil (5 290 S) (Silva et al., 2012; Dantas Ceara et al., 2013). During their migration, Magellanic penguins seem to

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be vulnerable to a number of environmental disturbances, which includes exposure to and accumulation of environmental pollutants, such as oil and heavy metals (Gandini et al., 1994; Keymer et al., 2001; García-Borboroglu et al., 2006; Gil et al., 2006; Vega et al., 2010; Godoy et al., 2014; Kehrig et al., 2015; Tavares et al., 2017). Persistent toxic chemicals, such as mercury (Hg), pose great concern to marine ecosystems due to their incorporation into the marine food web, threatening particularly long-lived and/or high trophic predators at the individual and population levels, through bioaccumulation and biomagnification processes (Monteiro and Furness, 1995; Elliot and Scheuhammer, 1997; Wolfe et al., 1998; Brasso and Polito, 2013). Although Hg has natural sources in the environments, historical human activities have increased emissions to the ecosystems, modifying its global cycling mechanisms (Driscoll et al., 2013). Subsequently, bioavailable Hg levels have increased in the marine environments, threatening a vast and diverse list of organisms (Robinson et al., 2009; Driscoll et al., 2013). Mercury concentrations in penguins, including S. magellanicus, are expected to be low given the remote environment where most species inhabit, located far from the main emission sources of chemical pollutants (Brasso et al., 2015). In this respect, Bratkic et al. (2016) reported low Hg concentrations in South Atlantic waters around 40 S latitude, which considerably matches with the breeding location of Magellanic penguins on the Argentina coast. Nevertheless, previous studies have reported harmful hepatic Hg concentrations in Antarctic penguins. As an example, Szefer et al. (1993) reported an average concentration of 34.7 mg g1 dry weight in hepatic tissues of Gentoo penguins (Pygoscelis papua) surpassing even measurements from other marine mammal species assessed in the same study, such as crabeater (Lobodon carcinophagus) and the leopard seals (Hydrurga leptonyx). Gill and Darby (1993) also detected hepatic Hg concentrations ranging 6.81 mg g1 wet weight in yellow-eyed penguins (Megadyptes antipodes) from New Zealand. Other scientific studies have also reported on Hg concentrations in tissues from several penguin species from different breeding grounds, including S. magellanicus (Gil et al., 2006; Vega et al., 2010; Frias et al., 2012; Kehrig et al., 2015). Gil et al. (2006), for example, analyzed toxic metals in seabirds (e.g. penguins, gulls, petrels, albatrosses and other waterbirds) sampled on the Patagonian coast of Argentina, and found that Hg concentrations were higher in Magellanic penguins when compared with other examined species. It is important to highlight that biological factors known to influence the Hg concentrations in large marine vertebrates, such as age, could bias the comparison within and among species (Stewart et al., 1997). Juvenile penguins spend considerable energy in their migration along the South American waters, which compromises their body condition and may influence the accumulation of persistent elements. Indeed, most animals recovered from beaches along the Brazilian coast display clear signs of starvation (Dantas et al., 2013) and the evaluation of stomach contents (Di Beneditto et al., 2015) supports this observation. What is not well investigated, and is the main focus of this current research, is how Hg concentrations can vary along the migration path and across the annual wintering nonbreeding periods of juvenile Magellanic penguins. The aim of this research is to investigate the variability of Hg concentrations in juvenile Magellanic penguins found dead stranded in different annual wintering periods and along their latitudinal migrating path on the Brazilian coast. As body condition is a determinant biological trait linked to migration performance in birds (Duijns et al., 2017), we also considered this as a research variable that might be associated to the Hg concentrations in the

sampled penguin specimens. 2. Materials and methods 2.1. Sample collection Hepatic and muscle tissues were obtained from juvenile Magellanic penguins found dead stranded along the Brazilian coast during their wintering journey along the Atlantic waters of South America. The sampling activities were conducted during a daily beach monitoring survey following a standardized protocol aiming to collect information and biological samples from stranded marine megafauna (Moura et al., 2016; Tavares et al., 2016). Only fresh dead specimens were selected for tissue analyses, generally presenting normal appearance, fresh smell and dark red and firm muscle tissues, corresponding to the code 2 of the protocol reported by Geraci and Lounsbury (2005). All specimens sampled in this study presented juvenile plumage characteristics (Boersma et al., 2013). Indeed, it has been observed that over 95% of the Magellanic penguins undertaking long-distance wintering migration are juveniles (García-Borboroglu et al., 2010; Reis et al., 2011). We assessed the variability of Hg concentrations in samples of stranded penguins collected at three latitudinal areas along the Brazilian coast for the year 2008: Rio Grande do Sul (Lat. 31000 S), Rio de Janeiro (Lat. 22 500 S) and Sergipe (Lat. 11000 S) (Fig. 1). With this part of the study design, we aimed to evaluate to which extent the fitness and energetic imbalance linked to the distance reached from the breeding grounds can be associated with Hg concentrations in juvenile penguins. Nevertheless, the specific breeding populations from where the sampled penguins belong to, and from where they began their northward migration along the Atlantic coast of South America are unknown. Therefore, the samples from 2008 were collected in a time frame of two days in order to reduce the chance that the sampled penguins come from very distant and

Fig. 1. Map displaying the three latitudinal sampling areas for Magellanic penguins (Spheniscus magellanicus) along the Brazilian coast. In the bottom right corner is a graphical representation of a characteristic juvenile penguin sampled herein. Rio ¼ Rio de Janeiro; R.Sul ¼ Rio Grande do Sul.


distinct breeding locations, what could bias the latitudinal comparison. In order to investigate the annual variation of Hg concentrations in the juvenile penguins during their migration, we used samples collected on the beaches of the state of Rio de Janeiro across three wintering migration periods: 2006, 2008 and 2012. The data from 2006 were extracted from Vega et al. (2010), who studied the differences in metal concentrations between juvenile penguins collected in southeastern and southern Brazil. Breast muscle and liver tissues were selected to enable comparisons with the results from Vega et al. (2010). Therefore, we follow similar sampling and analytical procedures conducted by those authors. Moreover, many studies addressing Hg accumulation in penguins and other flying seabirds species have been conducted using muscle and liver tissues as the biological matrix under investigation (Lock et al., 1992; Gill and Darby, 1993; Szefer et al., 1993; Moreno et al., 1997; Bargagli et al., 1998; Keymer et al., 2001; Gil et al., 2006; Smichowski et al., 2006; Choong et al., 2007; Vega et al., 2010; Kehrig et al., 2015). Hg analyses in penguin liver and muscle tissues will allow us to conduct a comparative approach to enable us to highlight important issues concerning Hg concentrations in our target species. Seabird livers display important biochemical functionalities to cope with chemical pollutants, including storage, redistribution, detoxification, and transformation (Burger and Gochfeld, 2004). Normally, penguins show the ability to accumulate high Hg concentrations in the liver, primarily transferred from their prey (Monteiro and Furness, 1995; Furness and Camphuysen, 1997). The mortality causes of the penguins were not determined, although in most cases the individuals were visually emaciated and dehydrated, as previously reported in other studies (GarcíaBorboroglu et al., 2010). During migration, penguins are subjected to a challenging energetic demand that generally progresses to a severe malnourishment condition (Dantas et al., 2013). Frequently, body condition is negatively associated with Hg concentrations in seabirds, as the energetic demand during migration induces the organism to catabolize lean tissues causing a mobilization of Hg in the body and exacerbating the concentration in tissues (Anteau et al., 2007; Seewagen et al., 2016). Therefore, body condition was used as a metric to investigate its effect on Hg concentration in liver and muscle of penguins. Samples of liver and muscle tissues, weighing approximately 10 g per individual sample, were extracted and immediately frozen at 20 C for further laboratory analyses. Data on body length (maximum straight length between the tips of the bill and the tail) and body weight were also recorded in order to investigate the influence of body condition on the Hg levels detected in penguins. We used these body measurements to determine a morphometric estimation of body condition that can more satisfactorily be applied as a proxy for the mass of body fat, essential for migratory birds (Labocha and Hayes, 2012). For this purpose, we calculated the index ratio of weight (Kg) over length (cm) of the penguins, to reduce the influence of size variation in the data, although all individuals belong to the same juvenile age class. 2.2. Analytical methods For consistency regarding the comparative assessment, the Hg quantification method in Magellanic penguin tissues was performed following the same sample preparation described by Vega et al. (2010). All samples were defrosted and homogenized with a food microprocessor (Black & Decker HC31). Approximately 0.5 g of tissue was weighed, and digested with a 1:1 mixture of sulphuric and nitric acid, in the presence of 0.1% vanadium pentoxide. The digestion temperature was 80 C, and

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oxidation was completed by the addition of a sufficient volume of 5% m/v potassium permanganate solution. Immediately before the instrumental analysis, the oxidant excess was reduced with a 20% m/v solution of hydroxylammonium chloride, diluted to 50 mL. The quantification process was conducted with an inductively coupled plasma mass spectrometry (ICP-MS), using a Perkin Elmer NexIon 300X spectrometer. The sample introduction system consisted of a Meinhard-type nebulizer with a twister cyclonic chamber. During the analysis, 103Rh was used as internal standard at a concentration of 20 mg L1. To ensure the accuracy of the analytical method, a certified reference material for Hg from the National Research Council of Canada (DOLT-3, dogfish liver sample) was analyzed in parallel, using the same digestion process applied to the samples. The variation obtained with the certified reference material was lower than 10 percent, ensuring the accuracy and precision of Hg determination in the tissues. All Hg concentrations are computed here on a mg g1 wet weight (w.w.) basis. 2.3. Data analysis We assessed the contribution of the variables of body condition index, sampling areas along the migration path (for 2008) and wintering migratory periods (years) on the muscle and hepatic Hg concentrations through an analysis of covariance (ANCOVA). We analyzed the Hg concentrations as functions of body condition index as covariates in the ANCOVA models. The ANCOVA analyses were computed separately for muscle and hepatic tissues and for each categorical factor (areas and years), resulting in four independent models. The data was log-transformed to fit it with the ANCOVA assumptions of normality and homogeneity of residuals (Crawley, 2012). Following up the ANCOVA statistical results, Tukey post hoc tests were implemented to assess the pairwise comparison between the adjusted Hg means across the years and latitudinal regions. The level of significance for the statistical tests was based on p < 0.05. All the statistical analyses were performed using R language and software. More details on the statistic metrics can be found in the supplementary material of this paper. 2.4. Results The overall total length and body weight of the juvenile penguins varied respectively from 49 to 70 cm (61.12 ± 3.60) and 1.5 to 3.9 kg (2.13 ± 0.42), while Hg concentrations ranged from 0.1 to 9.7 (1.82 ± 1.61) in the liver and 0.1 to 2.0 (0.47 ± 0.28) mg g1 w.w. in the muscle. Penguin body condition indices differed significantly among the three years (f ¼ 5.66, p < 0.01). Those penguins with higher body condition indices stranded more often during the wintering period of 2006, with a decreasing trend toward the subsequent two sampling years for the Rio de Janeiro state. However, a significant comparison was observed only between 2006 and 2012 (t ¼ 3.29, p < 0.05) (Fig. 2). The ANCOVA analyses for the three wintering years revealed that hepatic Hg levels were significantly correlated with body condition indices (f ¼ 4.88, p < 0.05) in the Magellanic penguins (SI Table S2). Similar results were obtained considering the ANCOVA test for muscle Hg concentrations, which were also significantly related to the body condition index (f ¼ 14.67, p < 0.001) (SI Table S2). Significant effects of the three migration years on the Hg concentrations in liver (f ¼ 12.34, p > 0.001) and muscle (f ¼ 7.85, p < 0.001) were observed, after controlling for the effects of body condition index. The Tukey post hoc tests indicated that the covariate-adjusted mean for hepatic Hg in 2012 was significantly lower than those for 2008 (t ¼ 4.92, p < 0.001) and 2006 (t ¼ 3.25, p < 0.005) (SI Table S3). The post hoc test considering muscle Hg levels also indicated that individuals in 2008

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tissues collected along the Rio de Janeiro, followed by the Sergipe and Rio Grande do Sul coasts. 3. Discussion

Fig. 2. Latitudinal (left column, Areas) and annual (right column, Years) comparison for hepatic and muscle Hg levels and for body condition index in Magellanic penguins (Spheniscus magellanicus) stranded along the Brazilian coast. The latitudinal includes only penguins sampled during 2008, whereas for the annual comparison presents only those animals stranded along the Rio de Janeiro coast, Brazil. Rio ¼ Rio de Janeiro; R. do Sul ¼ Rio Grande do Sul.

presented significantly higher Hg concentrations than in 2006 (t ¼ 3.27, p < 0.005) and 2012 (t ¼ 3.64, p ¼ 0.005), after controlling for the effect of body condition (SI Table S3). No significant results were obtained for the comparison of the adjusted mean of Hg levels between 2006 and 2012 in muscle and between 2006 and 2008 in liver tissues. The body condition indices of the stranded penguins differed significantly across the three sampling areas along the Brazilian coast (f ¼ 11.15, p ¼ 0.001). The penguins found stranded at the northernmost region (Sergipe) presented significantly lower body condition indices when compared to those birds sampled in the two other areas (Rio de Janeiro t ¼ 4.18, p < 0.001; Rio Grande do Sul t ¼ 4.24, p < 0.001). No substantial differences were observed and statistically supported for the mean body condition indices between Rio Grande do Sul and Rio de Janeiro (Fig. 2 and SI Table S1). The ANCOVA analyses concerning the effects of latitudinal areas on Hg concentrations also indicated a significant relationship of hepatic Hg levels with the covariate body condition index (f ¼ 4.92, p < 0.05). After accounting for the effect of the covariate body condition, the results of the ANCOVA model indicated statistically significant differences for the mean Hg concentrations in liver across the sampling areas (f ¼ 5.21, p < 0.01). The adjusted mean of hepatic Hg concentration was significantly higher in samples from penguins found stranded on the southernmost region (Rio Grande do Sul) compared to the two other northern sampling stations (Rio de Janeiro t ¼ 3.09, p < 0.01; Sergipe t ¼ 2.31, p < 0.05). No significant differences in muscle Hg concentrations across the latitudinal sampling zones were observed, although slightly higher concentrations were observed in penguins

Variations in Hg concentrations in seabirds can be attributed to many factors, including feeding and migratory habits, as well as body condition (Monteiro and Furness, 1995; Polito et al., 2016). In our study, we observed a decline in body condition indices as we move from the nearest (Rio Grande do Sul) towards the farthest (Sergipe) sampling areas from the penguins breeding grounds. This may reflect the energetic demand of the migration as the individuals swim further from the breeding localities (Silva et al., 2012). The most significant difference in Hg concentrations in livers of juvenile Magellanic penguins was between the southernmost (Rio Grande do Sul) and the other two northern sampling locations. The southernmost sampling area, the nearest from the breeding region, presented both the highest Hg levels in liver and body condition indices. Moreover, our wintering comparison demonstrated that penguins sampled in 2012 presented both the poorest body condition indices and the lowest Hg concentrations in ska et al. (2010) found that mercury muscle and liver tissues. Kalisin concentrations were considerably higher in the common merganser (Mergus merganser) classified as displaying good body condition, during the wintering period at Poland region. The authors suggest that birds with good body condition are likely to be more efficient hunters and, consequently, consume higher amounts ska et al., 2010). On the other hand, of Hg-containing preys (Kalisin Scheuhammer et al. (1998) found higher Hg concentrations in liver, kidney, and muscle from emaciated aquatic birds (Gavia immer and Mergus merganser) compared to those individuals with normal body condition. Normally, declines in body condition have been linked to increasing Hg levels in some captive and wild aquatic birds (Anteau et al., 2007). For example, body condition was negatively related to and affected by Hg concentrations in tissues of California clapper rails (Rallus longirostris obsoletus) sampled from marsh environment of San Francisco Bay (Ackerman et al., 2012). The data modeling approach of that study indicated a potential decrease in body mass over the observed range of Hg concentrations in blood, feather, and eggs. Giving the high energetic cost to perform the migration and the relatively low Hg levels detected in the samples of Magellanic penguins from our study, it is more likely to assume that body condition was the factor influencing the variability in Hg concentration, not the reverse condition. However, the combination of poor body condition and Hg accumulation during the migration period might be particularly critical for penguins in the juvenile age phase. Magellanic penguins from the Patagonian breeding population begin hatching at middle November, and in April they start their migration, therefore the age of juvenile specimens sampled in this study may vary from 8 to 10 months old (Scolaro, 1987; Yorio et al., 2001). It is important to highlight that the penguins with higher body condition indices in our study cannot be interpreted as having good body condition. Although the sampling activities were carefully conducted, a selection bias may exist, as the stranded organisms may not represent the migratory community. Our results indicate that the highest Hg levels were detected in the specimens sampled in 2008 along the Rio de Janeiro coast. During the northward winter migration along the Southwest Atlantic, Magellanic penguins may experience extensive metabolic shifts due to changes in prey availability and also as a result of trophic imbalance linked to environmental changes (Bond and Diamond, 2008; Silva et al., 2012). An extreme die-off episode of juvenile Magellanic penguins occurred in 2008 throughout their migratory path along the Atlantic coast of South America (Silva


et al., 2012; Dantas et al., 2013). There is scientific evidence indicating that this atypical mortality period may have been triggered by the pressure of an anomaly in the sea surface temperature on the trophic structures, which may have affected penguin prey availability, resulting in lack of fitness prior and during the migration journey (García-Borboroglu et al., 2010; Silva et al., 2012; Dantas et al., 2013). A malnourishment condition linked to trophic imbalance caused by environmental changes may influence Hg assimilation and bioaccumulation in penguins and other seabirds ska et al., 2010). Nevertheless, although higher Hg levels (Kalisin were found in penguins sampled in 2008, the selected individuals did not present the lowest body condition indices compared to individuals sampled during other years. Studies on Hg accumulation in penguins indicate that, in general, those species displaying a more limited distribution range in the Antarctic region, such as the Chinstrap penguin Pygoscelis antarcticus (Norheim et al., 1982) and the Adelie penguin Pygoscelis adeliae (Szefer et al., 1993; Moreno et al., 1997; Smichowski et al., 2006), present low Hg concentrations. Other penguin species, presumably not alarmingly exposed to human-related pollution presented considerable high Hg levels, such as the Gentoo penguin Pygoscelis papua (Szefer et al., 1993) and the yellow-eyed penguin Megadyptes antipodes (Lock et al., 1992; Gill and Darby, 1993). The interspecific variations in Hg accumulation in penguin and other seabird species may reflect differences in their trophic properties, regional contamination and physiological aspects (Kojadinovic et al., 2007). In general, penguins present low Hg accumulation compared to other Antarctic and Subantarctic flying seabird species. For example, Lock et al. (1992) found significantly high mean Hg levels in liver tissues of pelagic feeding seabirds, including: whitechinned Petrel (Procellaria aequinoctialis; 34 mg g1 w.w.), lightmantled albatross (Phoebetria palpebrata; 145.8 mg g1 w.w.) and wandering albatross (Diomedea exulans; 295.0 mg g1 w.w.). High Hg levels have also been detected in several other species inhabiting the Antarctic ecosystem (Thompson et al., 1993; Bargagli, vin et al., 2013; Wintle et al., 2015), and, despite the 2008; Ble remoteness regarding human related Hg sources, there is evidence to suggest that anthropogenic emissions are inducing the increasing of Hg levels in the region (Cossa et al., 2011; Lamborg et al., 2014) and, probably, its incorporation in the marine biota (Bargagli et al., 1998; Bargagli, 2008). Indeed, Goutte et al. (2014) reported an inverse relationship between breeding success and blood Hg levels in South Polar Skua (Catharacta maccormicki) and Brown Skuas (C. lonnbergi) from Sub Antartic Islands. Although the later species exhibited lower Hg levels it suffered from higher Hginduced breeding failure. Some seabirds seem to tolerate high levels of Hg, apparently due to their mechanisms of detoxification to cope with the accumulation of this toxic metal (Monteiro and Furness, 1995). For example, seabirds, including penguins, can eliminate a considerable body burden of Hg through moulting, by removing the feathers containing high Hg levels mobilized from other tissues (Monteiro and Furness, 1995; Pedro et al., 2015). Moreover, seabirds and other marine mammals can use available selenium (Se) to demethylate methylmercury, one of the most toxic forms of Hg, into an HgSe complex with inert, non-toxic functions to the organism (Dietz et al., 2000; Ikemoto et al., 2004). Therefore, there is a limitation on using information of Hg levels alone to interpret the toxic effect of this metal on the birds without assessing the parameters linked to the detoxification in the organisms. Juvenile Magellanic penguins feed mainly upon cephalopod species during the migration period along the Brazilian coast, especially the pelagic octopus Argonauta nodosa (Di Beneditto et al., 2015). Usually, cephalopods are not important Hg vectors to their

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predators when compared to fish, as demonstrated by some trophic studies conducted in the marine environment (Bisi et al., 2012; Di Beneditto et al., 2015). Therefore, it is expected to detect relatively low Hg concentrations in juvenile specimens along with their migration path. Moreover, the food remains in the stomach chambers are typically composed of resistant fragments of ingested prey, which indicate that these penguins may not forage regularly during their migration period in Brazilian waters (Baldassin et al., 2010). Consequently, the detected Hg concentrations may represent exposure in areas closer to their breeding areas. 4. Conclusions Body condition is an important factor related to Hg concentrations in both hepatic and muscle tissues of juvenile Magellanic penguins during their wintering migration along South Atlantic. However, further investigation is required in order to understand how Hg concentrations in juvenile penguins in their breeding grounds vary according to time and distance as they move during their migration path. The concentrations detected in our sampled penguins may not indicate an alarming risk condition. However, chemical pollutants, even at relatively low concentrations, may be a special health issue to juvenile penguins in a critical nourishment condition during their migration. Our study indicates that the higher Hg concentrations throughout the sampling years was observed for 2008, coinciding with an atypical die-off episode of the species reported in that year, possibly caused by the impact of environmental changes on trophic structure (García-Borboroglu et al., 2010). Further studies on Hg concentrations in penguins could account for a combination of factors, including shifts in trophic signals and environmental attributes that can influence productivity along their migration path. Acknowledgements We would like to thank the team from the Grupo de Estudos de Mamíferos Marinhos da Regi~ ao dos Lagos (GEMM-Lagos) for undertaking the activities and CENPES/PETROBRAS for managing the Habitats Project Campos Basin Environmental Heterogeneity, which included this study. D.C. Tavares acknowledges CAPES for providing research grant to visit the Leibniz Centre for Tropical Marine Research. J.F. Moura gratefully acknowledges CAPES and the Alexander von Humboldt Foundation for financial support (Proc. BEX 0128/14-7), as well as the Deutscher Akademischer Austauschdienst e DAAD (57384894/08). Appendix A. Supplementary data Supplementary data related to this article can be found at https://doi.org/10.1016/j.envpol.2018.03.021. References Ackerman, J.T., Overton, C.T., Casazza, M.L., Takekawa, J.Y., Eagles-smith, C.A., Keister, R.A., Herzog, M.P., 2012. Does mercury contamination reduce body condition of endangered California clapper rails? Environ. Pollut. 162, 439e448. https://doi.org/10.1016/j.envpol.2011.12.004. Anteau, M.J., Afton, A.D., Custer, C.M., Custer, T.W., 2007. Relationships of cadmium, mercury, and selenium with nutrient reserves of female lesser scaup (Aythya affinis) during winter and spring migration. Environ. Toxicol. Chem. 26, 515e520. https://doi.org/10.1897/06-309R.1. Baldassin, P., Santos, R.A., Cunha, J.M.M., Werneck, M.R., Gallo, H., 2010. Cephalopods in the diet of Magellanic penguins Spheniscus magellanicus found on the coast of Brazil. Mar. Ornithol. 38, 55e57. Bargagli, R., 2008. Environmental contamination in Antarctic ecosystems. Sci. Total Environ. 400, 212e226. https://doi.org/10.1016/j.scitotenv.2008.06.062. Bargagli, R., Monaci, F., Sanchez-Hernandez, J.C., Cateni, D., 1998. Biomagnification of mercury in an Antarctic marine coastal food web. Mar. Ecol. Prog. Ser. 169,

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