Marine Pollution Bulletin 91 (2015) 410–417
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Mercury accumulation in sediments and seabird feathers from the Antarctic Peninsula Paola Calle a,⇑, Omar Alvarado a, Lorena Monserrate b, Juan Manuel Cevallos b, Nastenka Calle c, Juan José Alava d a
Escuela Superior Politécnica del Litoral, Facultad de Ciencias Marítimas, Oceánicas y Recursos Naturales, Guayaquil, Ecuador Escuela Superior Politécnica del Litoral, Centro de Investigaciones Biotecnológicas del Ecuador, Guayaquil, Ecuador Pacific Institute for Climate Solutions, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A1S6, Canada d School of Resource & Environment Management, Faculty of Environment, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A1S6, Canada b c
a r t i c l e
i n f o
Article history: Available online 22 November 2014 Keywords: Mercury Sediment Seabirds BMF BSAF
a b s t r a c t In an effort to assess the impact of mercury in the Antarctic Peninsula, we conducted ecotoxicological research in this region during the summer of 2012 and 2013. The objectives were to assess: (a) mercury levels in sediment samples; (b) mercury accumulation in Antarctic seabird feathers: Catharacta lonnbergi (brown skua), Pygoscelis papua (gentoo penguin) and Pygoscelis antarctica (chinstrap penguin); and (c) biomagnification (BMF predator/prey) and biota sediment accumulation (BSAF skuas/sediment) factors. Mercury concentrations in sediment were relatively low. Mercury concentrations were significantly higher in brown skuas and gentoo penguins than in chinstrap penguins (2012), and significantly higher in brown skuas than in both penguins (2013). BMF indicated 2–7.5 times greater mercury levels in brown skuas than in penguins. BSAF values suggested an apparent temporal decrease of 18.2% of this ratio from 2012 to 2013. Long-range environmental transport is the likely route of entry of mercury into the Antarctic Peninsula. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction The Antarctic continent is one of the few regions on the planet that is still considered a pristine environment; therefore, it is of particular importance to preserve this unique region. However, there are several studies that have given warning signals of possible contamination and degradation of the Antarctic environment by anthropogenic pollutants, including relatively high metal concentrations at various trophic levels of the regional marine food web (Bargagli et al., 1998; Metcheva et al., 2006; Jerez et al., 2011). Other studies have demonstrated that due to its high volatility and long residence time, mercury (Hg) can reach remote areas of the planet through long range atmospheric transport (Nriagu, 1989; Fitzgerald et al., 1998; Lindberg et al., 2007). Atmospheric Hg is predominantly the gaseous elemental form (Hg0), which can be oxidized to HgII and then deposited. It is estimated that more than 80% of the Hg deposited in the ocean is re-emitted to the atmosphere as Hg0, driving the cycle of Hg through biogeochemical reservoirs (Strode et al., 2007). The half-life of atmospheric Hg0 in polar regions is short (Driscoll et al., 2007), but ⇑ Corresponding author. E-mail address: [email protected] (P. Calle). http://dx.doi.org/10.1016/j.marpolbul.2014.10.009 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
once Hg0 is deposited in aquatic ecosystems, it can be methylated by microorganisms to form methylmercury (Me–Hg). Me–Hg is highly toxic and bioaccumulates throughout the food web almost entirely via dietary uptake, reaching the highest concentrations in organisms at the top of the food web (Wiener et al., 2007). Seabirds have been successfully used worldwide as indicators of environmental contamination (Furness and Camphuysen, 1997; Walsh, 1990) because they exhibit different trophic levels and they have long life spans (Walsh, 1990). Seabirds can accumulate bioavailable forms of contaminants and species at high trophic levels can biomagnify contaminants to concentrations that are several orders of magnitude higher than the concentration in the environment (Burger and Gochfeld, 2000; Roomen et al., 2006). Seabird feathers have been employed as indicators of metal contamination in the environment because metals are sequestered in feathers during the birds’ growing phase (Burger, 1993) and seabirds eliminate metals through their feathers during molting (Burger, 1993: Hughes et al., 1997). In the case of Hg, the concentration of Hg in feathers has been shown to correlate with those in internal tissues (Thompson et al., 1990, 1991). Therefore, the use of feathers represents a noninvasive approach for monitoring mercury accumulation in seabirds and the marine environment (Appelquist et al., 1984; Furness et al., 1986; Thompson et al., 1990; Bond and
P. Calle et al. / Marine Pollution Bulletin 91 (2015) 410–417
Diamond, 2009). Data for mercury in seabird feathers are substantial for the North Pacific, North Atlantic and Arctic regions (Norheim, 1987; Thompson and Furness, 1989a,b; Thompson et al., 1990; Thompson et al., 1998a,b; Bearhop et al., 2000; Savinov et al., 2003; Burger et al., 2007; Bond and Diamond, 2009). Data on mercury in seabirds from the Southern Ocean and Antarctica like Antarctic penguins, brown skuas and albatrosses (Norheim et al., 1982; Thompson and Furness, 1989a,b; Ancora et al., 2002; Becker et al., 2002; Metcheva et al., 2006; Jerez et al., 2011; Blevin et al., 2013), and for seabirds from the Chilean and Argentinean coasts (Ochoa-Acuña et al., 2002; Frias et al., 2012) are gradually emerging. The aim of the present study was to assess ambient Hg levels and Hg bioaccumulation in seabirds in the Antarctic Peninsula. Specifically, this study aimed to: (a) determine concentrations of mercury in sediment and in feathers samples of the Greenwich and Barrientos Islands; and, (b) assess mercury accumulation in feathers of Antarctic seabirds, including penguins (Pygoscelis papua and P. antarctica) and brown skuas (Catharacta lonnbergi). Sampling for this study was done during the XVI and XVII EcuadorianAntarctic expeditions to Ecuador’s Scientific Station ‘‘Pedro Vicente Maldonado’’ at the Antarctic Peninsula carried out by the Ecuadorian Antarctic Institute (INAE). 2. Materials and methods 2.1. Study area The study area encompasses the Greenwich and Barrientos Islands of the Antarctic Peninsula. Greenwich Island is located at 62°310 S, 59°460 O and harbors the Ecuadorian Research Station ‘‘Pedro Vicente Maldonado’’ (i.e. Punta Fort Williams). Sampling was conducted around the station using three tracks established by the Ecuadorian Station to access the coastline of Punta Fort Williams, which enclose two sampling sites: Ensenada Guayaquil and Bahia Chile. This sector of the island is used only by the technical and military personnel that work at the Station and visiting scientists that come to the island for research purposes. Barrientos Island is located at 62°420 S, 59°470 O, and is used principally as a tourist stopover for cruise ships where tourists land and walk around the island for birdwatching. Sampling at this island was deployed around its coastline (Fig. 1). All sampling was done during the Antarctic summer and seabird breeding seasons of 2012 and 2013. A total of eleven sampling sites were surveyed for Punta Fort Williams and seven sites for Barrientos Island (Fig. 1). 2.2. Samples collection Samples of sediment were collected from eighteen locations in the Antarctic Peninsula including Ensenada Guayaquil (n = 6 sites) and Bahia Chile (n = 5 sites) of Greenwich Island and seven sampling sites of Barrientos Island (Fig. 1). Sediment samples ( 5 cm deep) were collected using a small plastic shovel and placed in Ziploc-type plastic bags. Sediment was stored at 4 °C until transportation to the laboratory in Ecuador for about one month. Once in the laboratory each sediment sample was homogenized and dried using a conventional oven at 70 °C for 48 h. Dried sediment samples (40 g) were pulverized using clean acid washed mortar and pestle. Pulverized sediment samples were stored in the desiccator until total mercury analysis. Three species of seabirds, gentoo penguins (P. papua), chinstrap penguins (P. antarctica) and brown skuas (C. lonnbergi), that inhabit the Antarctic Peninsula were identified as potential bio-indicators of Hg contamination. Hg binds strongly to the sulphydryl groups of feathers’ keratin (i.e. a high molecular weight fibrous, structural
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protein), within which organic mercury (i.e. Me–Hg) is highly stable and resistant to environment factors such as ultraviolet light, heat, freezing and weathering (Appelquist et al., 1984). Molted feathers were collected randomly in and around nests and colonies of penguins aggregated on Barrientos Island and skuas from Punta Fort Williams. While collected feathers for skuas (i.e. primary feathers) were from adult individuals, molted feathers for penguins were from chicks. Samples were brought to the laboratory of Maldonado Station and rinsed with pure acetone, followed by a generous rinse with deionized water (Burger and Gochfeld, 2000). Feathers were air dried at 20 °C, after which they were wrapped in acetone-rinsed aluminum foil and stored in the freezer (18 °C) until analysis. While the major purpose of the analysis was to measure the whole feather, we also investigated whether concentrations of Hg exhibit variation along the feather’s length. Therefore, three feathers from brown skuas (Feather 1: 33 cm; Feather 2: 22.5 cm; Feather 3: 18.0 cm) collected in 2013 where cut and analyzed in four sections from the calamus or quill (region 1) located at the base of the feather, through regions 2 and 3, to the tip of the feather rachis (region 4), as illustrated in Fig. 2. 2.3. Mercury analysis Total mercury in sediment and seabird feathers of the Antarctic Peninsula was determined via atomic absorption spectrophotometry using a Direct Mercury Analyzer (DMA-80). The advantage of using this equipment is that the instrument does not require acid digestion of the sample or other pretreatment. Because great amount of mercury in feathers is present in the form of Me–Hg, a measurement of total mercury concentration was used as a proxy of this bioavailable form (Thompson and Furness, 1989a, 1989b). The limit of detection of the equipment was 0.005 ng. Quality control and assurance was performed by analyzing the concentration of the standard reference material (SRM)-1646a Estuarine Sediment (NIST) and procedural blanks in each set of sediment and feathers samples analyzed. SRM recoveries were >94% for the 2012 samples and >93% for the 2013 samples (Table 1). For sediment samples, blanks had mean concentrations ranging from 0.0008 to 0.0015 mg/kg dw, while mean concentrations for blanks run with feathers ranged from 0.0010 to 0.0015 mg/kg dw (Table 1). All mercury concentrations are expressed as dry weight (mg/kg dw) (See Table 2). 2.4. Data treatment and statistical analysis Concentrations of mercury measured were blank-corrected using the method detection limit (i.e. MDL), defined here as the mean response of concentrations measured in n = 3 and n = 5 procedural blanks analyzed in the same run as the sediment and seabird feather samples, respectively. Most mercury concentration data were normally distributed as tested by the Shapiro–Wilk W test (p > 0.05), except for concentrations observed in skua feathers collected in 2012 and sediments from Bahia Chile collected in 2013, which were not normally distributed (Shapiro–Wilk W test, p < 0.05). Differences in contaminant concentrations among sites and seabird species were evaluated using analysis of variance (ANOVA) when variances among sites or seabird species were equal (i.e. homoscedastic as tested by the Bartlett test, p > 0.05), or Welch ANOVA when variances were unequal (i.e. heteroscedastic; Bartlett test, p < 0.05) for normally distributed data. These statistical comparisons were followed by a Tukey–Kramer honestly significant difference (HSD) multiple comparison test, which is a post hoc method recommended to test differences between pairs of means among groups that contain unequal sample sizes (Zar, 1999). Alternatively, a nonparametric test (Kruskal–Wallis test)
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Fig. 1. Geographical location of sampling sites at the Greenwich and Barrientos Islands in the Antarctic Peninsula.
Region 1 (calamus)
Region 2
Region 3
Region 4 (rachis tip)
Fig. 2. Feather of a brown skua (C. lonnbergi) showing the subdivision of the four regions analyzed to assess the accumulation of mercury within and along the feather.
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P. Calle et al. / Marine Pollution Bulletin 91 (2015) 410–417 Table 1 Quality control and assurance measurements for analysis of reference material and procedural blanks.
a
Year
SRMa
n
Recovery% (mean ± SD)
Procedural blanks
n
Mean ± SD (mg/kg dw)
2012
Sediment Penguin Feathers Skua feathers
6 12 4
97.40 ± 2.50 94.00 ± 1.80 94.30 ± 3.60
Sediment Penguin feathers Skua feathers
18 24 9
0.0015 ± 0.0005 0.0012 ± 0.0001 0.0015 ± 0.0004
2013
Sediment Penguin Feathers Skua Feathers
6 12 4
95.50 ± 3.80 93.40 ± 1.60 94.30 ± 1.40
Sediment Penguin feathers Skua feathers
18 18 9
0.0008 ± 0.0002 0.0013 ± 0.0004 0.0010 ± 0.0001
SRM: standard reference material (SRM-1646a Estuarine Sediment, National Institute of Standardization and Technology, NIST).
for multiple comparisons was used when data did not fit a normal distribution. To determine differences in contaminant concentrations between samples collected in 2012 and 2013, either a Welch two-tailed t-test (for samples with unequal variances) or a t-test (for samples with equal variances) were used when data were normally distributed. The Wilcoxon rank-sum test was used as an alternative to the t-test when data did not follow a normal distribution. All statistical analyses were conducted using JMP 10.0 (2014 SAS Institute) at a level of significance of p < 0.05 (a = 0.05).
BMF > 1, i.e. a BMF greater than 1 indicates that the chemical is a bioaccumulative substance (Gobas et al., 2009). 2.6. Biota Sediment Accumulation Factor (BSAF) To investigate the species-habitat ecotoxicological relationship as a function of biota concentrations versus ambient concentrations (i.e. sediment or soil), the biota sediment accumulation factor (BSAF) was assessed as (Gobas and Morrison, 2000):
BSAF ¼ C B =C S
2.5. Biomagnification Factor (BMF) Because mercury biomagnification occurs in food webs, seabirds at the top of the food web are expected to accumulate higher concentrations of mercury than found in their diets or in animals at lower trophic levels. Biomagnification was expressed as the biomagnification factor (BMF) (Gobas and Morrison, 2000):
BMF ¼ C B =C D ; where CB is the concentration of mercury detected in the predator organism (i.e. brown skua) and CD is the concentration in the diet/ prey (i.e. Gentoo or chinstrap penguins). In this context, brown skuas are highly predatory seabirds feeding mainly on penguins, including eggs and mostly chicks (Reinhardt et al., 2000; Graña Grilli and Montalti, 2012), and mercury concentrations in these age categories are in turn expected to be similar to concentrations found in the parents (i.e. adult females) due to maternal transfer. Hence, the mercury levels in the feathers of penguins and brown skuas were used as surrogates for concentrations in the tissues of the whole organism, assuming that the birds had been exposed to mercury for a sufficiently long time for their Hg concentrations to reach a steady state (Gobas and Morrison, 2000). The criterion applied to indicate that mercury was biomagnified in skua was a
where CB is the chemical concentration in the predator (i.e. skua) and CS is the chemical concentration of sediment. We used mercury concentrations measured in skuas feathers and in sediments collected from Greenwich Island to determine BSAF values. A BSAF > 1 indicates the bioaccumulation potential of the chemical in relation to sediment levels (Gobas and Morrison, 2000; Arnot and Gobas, 2006). In addition, the BSAF is a bioaccumulation criterion used for ecosystem-based management purposes and as a risk assessment tool to provide potential sediment quality guidelines to protect organisms at the top of food webs (Alava et al., 2012). 3. Results 3.1. Sediments Mean concentrations of mercury ranged from 0.04 mg/kg dw in Barrientos Island to 0.06 mg/kg dw in Ensenada Guayaquil in 2012, and from 0.06 mg/kg dw in Ensenada Guayaquil to 0.20 mg/kg dw in Bahia Chile in 2013 (Fig. 3). No significant differences in total mercury sediment concentrations were found among sites in 2012 (ANOVA, df = 2, F = 1.94, p > 0.05), or among sites in 2013 (Kruskal–Wallis Test, df = 2, ChiSquare (v2) = 1.4605, p > 0.05), as
Table 2 Data for mercury concentrations in seabird feathers and sediment collected in 2012 and 2013 in the Antarctic Peninsula. Year 2012
2013
2012
2013
Sample
n
Mean ± SD (mg/kg dw)
Remarks
Seabirds: Gentoo feathers Chinstrap feathers Skua feathers
52 33 6
1.83 ± 0.80 0.83 ± 0.40 2.86 ± 2.60
Molted feathers Molted feathers Freshly fallen Feathers
Seabirds: Gentoo feathers Chinstrap feathers Skua feathers
18 18 3
0.49 ± 0.20 0.24 ± 0.01 1.80 ± 1.00
Molted feathers Molted feathers Freshly fallen Feathers
Sediment: Ensenada Guayaquil Bahia Chile Barrientos Island
6 5 7
0.060 ± 0.02 0.045 ± 0.03 0.040 ± 0.02
Surface sediment Surface sediment Surface sediment
Sediment: Ensenada Guayaquil Bahia Chile Barrientos Island
5 5 8
0.06 ± 0.02 0.20 ± 0.25 0.08 ± 0.02
Surface sediment Surface sediment Surface sediment
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shown in Fig. 2. Similarly, no temporal differences in mercury concentrations were detected in sediments collected in 2012 and 2013 (i.e. Bahia Chile: Wilcoxon test, df = 1, ChiSquare (v2) = 0.2727, p > 0.05; and, Ensenada Guayaquil, t-test, df = 9, p > 0.05) in the assessed areas, except for Barrientos Island, where mercury concentrations in sediments collected in 2013 were significantly higher than those measured in 2012 (t-test, df = 13, p < 0.05), showing a 50% increase in mean concentrations (Fig. 3).
6.00 5.00
Total Hg (mg/kg dw)
414
3.2. Seabird feathers
2012 2013
4.00
2.00
3.3. Variation in mercury concentration along the feather
A
A*
3.00
B*
1.00
Mean mercury concentrations in feathers ranged from 0.84 mg/ kg dw in chinstrap penguins to 2.90 mg/kg dw in brown skuas in the 2012 samples, and ranged between 0.20 and 1.80 mg/kg dw in chinstrap penguins and brown skuas in the 2013 samples (Fig. 4). Significant differences in total mercury concentrations were observed among feather samples collected from seabird species in 2012 (Kruskal–Wallis Test test, df = 2, ChiSquare (v2) = 16.58, p < 0.05). Mercury concentrations in chinstrap penguins (P. antarctica) feathers were significantly lower than those detected in Gentoo penguins (P. papua) and brown skuas (C. lonnbergi) (nonparametric multicomparison, Wilcoxon each pair, Z = 3.802, p < 0.05; and, Z = 2.85, p < 0.05, respectively). However, concentrations in Gentoo penguins were not significantly different from those observed in the brown skua (Wilcoxon test, Z = 0.492, p > 0.05). Similarly, significant differences in mercury concentrations were observed among feather samples collected from seabird species in 2013 (heteroscedasticity, Barlett test, p < 0.05; Welch ANOVA, p < 0.05); in the brown skua, mercury concentrations were significantly higher than the concentrations detected in Gentoo and Chinstrap penguins (Tukey–Kramer HSD test, p < 0.05), as shown in Fig. 4. Concentrations of mercury in feathers of Gentoo and chinstrap penguins collected in 2013 were significantly lower than those detected in 2012 (Gentoo: Welch t-test for unequal variances, p < 0.05; chinstrap: Welch t test for unequal variances, p < 0.05), as shown in Fig. 4. No significant differences in mercury concentrations were observed in the brown skua between 2012 and 2013 (Wilcoxon test, df = 1, ChiSquare (v2) = 0.0667, p > 0.05; Z = 0.129, p > 0.05).
A
B
B
0.00 Chinstrap pengüin
Gentoo pengüin
Brown skua
Fig. 4. Total mercury concentrations (mg/kg dw) in feathers of seabirds from the Antarctic Peninsula collected in 2012 and 2013. Concentrations in feathers not connected by the same letter differ significantly. Asterisks indicate significant differences between 2012 and 2013 for chinstrap and Gentoo penguins, respectively. Error bars are standard deviations.
feather rachis, but concentrations did not differ significantly among the regions of the feather sampled (Kruskal Wallis test, ChiSquare (v2) = 7.2051, df = 3, p > 0.05), as shown in Fig. 5. Although concentrations detected in the calamus (region 1) and regions 2 and 3 appear to be similar for all feathers (Fig. 5), high variation in mercury concentrations found in the tip (region 4) of the three feathers (i.e. mean ± SD = 3.80 ± 3.40 mg/kg dw, ranging from 1.20 mg/kg dw in feather 3 to 8.0 mg/kg dw in feather 1) may account for the lack of statistical significance. Similarly, when combining the mercury data from all regions of each feather to compare concentrations among feathers, no significant differences in mercury concentrations were observed among the three feathers of different sizes (Kruskal Wallis test, ChiSquare (v2) = 3.038, df = 2, p > 0.05), as illustrated in Fig. 6. 3.4. Mercury BMF The BMF values for the brown skua are reported in Table 3. The BMF for the brown skua/chinstrap penguin was higher than that determined for the brown skua/Gentoo penguin due to the lower concentrations of mercury observed in the chinstrap penguin relative to in the Gentoo penguins (Fig. 4). This indicates that mercury levels detected in brown skuas are 2–7.5 times greater than those found in these two species of penguins, which usually are prey for
Total mercury concentrations in brown skua feathers appear to increase from the calamus (region 1) to the tip (region 4) of the
8.00 7.00
2012 2013
Total Hg (mg/kg dw)
0.30
Total Hg (mg/kg dw)
0.25 0.20 0.15
*
0.10
6.00 5.00 4.00
Region 1 (calamus)
Region 2
Region 3
Region 4 (rachis tip)
3.00 2.00 1.00 0.00
0.05
1
2
3
4
Feather Region 0.00 Ensenada Guayaquil
Bahia Chile
Isla Barrientos
Fig. 3. Total mercury concentrations (mg/kg dw) detected in sediments collected from Barrientos Island and Greenwich Islands, Antarctic Peninsula, in 2012 and 2013. The asterisk indicates a significant difference between 2012 and 2013 for Isla Barrientos. Error bars are standard errors.
Fig. 5. Comparison and accumulation behavior of total mercury concentrations among regions of analyzed feathers (n = 3) in the brown skua. No significant differences in mercury concentrations across regions in the feathers were observed. Region 1 is the calamus at the base or lower part of the feather, while region 4 is the feather rachis tip at the top of the feather. Regions 2 and 3 are the segments found between regions 1 and 2.
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brown skuas in the region. Interestingly, an increase of about 55% in BMF values is observed from 2012 to 2013 in the study area, suggesting higher biomagnification factors in 2013 (Table 3). 3.5. Mercury BSAF The BSAF showed that mercury levels in the brown skua relative to those in sediments from Greenwich Island were 55.0–45.0 times (Table 3), and much higher compared to BMF values, indicating that concentrations of mercury in biota readily exceed ambient or abiotic (i.e. sediment) mercury concentrations and that there is a high potential transfer from sediment through the food web to apex predators. The BSAF was lower in 2013 when compared to the BSAF calculated for 2012, suggesting a temporal variability in the same area, underscoring the relatively lower concentrations of mercury found in skuas contrasting with higher mercury levels observed in sediments in 2013. 4. Discussion
Total Hg (mg/kg dw)
The lack of statistically significant differences in mercury concentrations in sediments among the sampling locations could be explained by a common global source of this pollutant. Local anthropogenic sources of mercury, which can be expected to produce differences in concentrations between human-inhabited stations (e.g., Ecuadorian Military/Navy Base, ‘‘Pedro Vicente Maldonado,’’ and several other international bases from different nations) in Greenwich Island and uninhabited islands (e.g., Barrientos Island), do not appear to be significant contributors to current sediment concentrations of mercury detected in the Antarctic Peninsula. This is further corroborated by the increase in sediment mercury concentrations found in Barrientos Island. Mercury inputs and deposition from global cycling, organic carbon content in sediments and variation in trophic transfer cannot be ruled out as factors influencing the temporal variation of mercury in biota and sediments in Barrientos Island as observed for the change in BSAF values from 2012 to 2013 (Table 3), which decreased to 70%. This appeared to be driven by higher mercury sediment concentrations in 2013 (Fig. 3) and low concentrations in skuas in the same year (Fig. 4). However, caution should be considered when interpreting this data because inter-annual variability may affect BSAFs and BMFs. Long terms studies and
Fig. 6. Box plots comparing the combined data for mercury concentrations measured in the four regions for three feathers of different lengths of the brown skua. The internal line across the middle of the box is the median; the ends of the box are the 25% and 75% quartiles; and the whisker bars are the minimum and maximum values. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Table 3 Biomagnification factor (BMF) for mercury in units of kg/kg wet weight using concentrations measured in feathers of the brown skua (predator) and two species of penguins (prey) and BSAF (skua/sediment) in units of kg/kg for Barrientos Island, Peninsula Antarctica. Year
2012 2013
BMF
BSAF
Brown skua/gentoo
Brown skua/chinstrap
Brown skua/sediment
1.60 3.60
3.40 7.50
55.0 45.0
monitoring are required to determine temporal trends in sediment and biota. The long-range transport capability of mercury species to remote areas of the world has been well documented (Fitzgerald et al., 1998; Nriagu and Pacyna, 1988; Nriagu, 1989; Mason and Sheu, 2002 AMAP, 2004; Lindberg et al., 2007; Søerensen et al., 2010). Long-range environmental transport comprising both atmospheric and oceanic processes is the likely route of entry of mercury into the marine environment of the Antarctic Peninsula and its wildlife. For instance, the short inter-temporal variation between 2012 and 2013 showed that mercury sediment concentrations in 2013 were 2.0 and 3.6 times the mercury concentrations in sediments collected in 2012 in Barrientos Island and Bahia Chile, respectively. This is of particular concern for the Antarctic environment, as mercury deposition to remote environments has increased by a factor of 3.0 since pre-industrial times (Lindberg et al., 2007). Our results show levels of mercury in penguin and skua feathers with significantly higher concentrations of mercury in gentoo penguins and brown skuas than those detected in chinstrap penguins. Metcheva et al. (2006) reported higher concentrations of several heavy metals in gentoo penguins than those detected in chinstrap penguins; however, mercury was not measured. Concentrations of mercury in chinstrap penguins were similar to previous concentrations reported for this species based on liver samples collected from specimens in Bouvetøya in the South Atlantic by Norheim et al. (1982) and Norheim (1987). Interspecific comparisons show that total mercury concentrations reported in this study for brown skuas, C. lonnbergi (2012: 2.86 ± 2.56 mg/kg dw; 2013: 1.80 ± 1.02 mg//kg dw) were lower than concentrations reported in great skua (Catharacta skua) feathers (6.34 ± 2.60 mg/kg dw) from Terra Nova Bay, Antarctica (Stewart et al., 1997). Our values are similar to concentrations reported in the Antarctic skua, Catharacta maccormicki (2.91 ± 1.93 mg/kg dw), from Shetland Islands (Bargagli et al., 1998) in Antarctica, and to that reported in one sample of the Chilean skua, Catharacta chilensis (i.e. 1.9 mg/kg dw) off the coast of Chile (Ochoa-Acuña et al., 2002). Total mercury concentrations in our seabirds were lower, comparable, and in some cases higher, relative to total mercury concentrations reported (ranging from 0.05 ± 0.01 to 5.31 ± 1.12 mg/kg dw) for 21 species of seabirds from the Subantarctic Zone (Kerguelen archipelago), Southern Ocean (Blevin et al., 2013). For instance, total mercury concentrations in our seabirds were lower than those detected in gray petrel (3.16 ± 1.21 mg/kg dw), wandering albatross (4.45 ± 1.60 mg/ kg dw), Subantarctic skua (5.15 ± 1.56 mg/kg dw) and Northern giant petrel (5.31 ± 1.12 mg/kg dw) from the Kerguelen archipelago (Blevin et al., 2013). Differences in metal concentrations in seabirds have been explained by the differences in diet and feeding habits among species (Thompson et al., 1998; Metcheva et al., 2006). Chinstrap penguin has been reported to feed exclusively on Antarctic krill, while gentoo penguin P. papua feeds on krill, fish and small squids (DelHoyo et al., 1992; McArthur et al., 2003). Methyl mercury is a highly lipophilic compound that can accumulate and biomagnify
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through the food web (Wiener et al., 2007). Prey fish are important in the transfer of MeHg to higher trophic levels (Wiener et al., 2007), which could explain the differences in Gentoo and chinstrap penguins. Biomagnification factors reported in this study indicate the mercury is been transferred from the prey to the predator (i.e. from Gentoo and chinstrap penguins to the brown skuas). While the variation in mercury concentrations within the feathers regions did not show a statistically significant increase from the calamus to the tip, there may be biological significance in terms of the tissue deposition and gradual accumulation of this metal in feathers as reflected by a relative increase in concentrations from the calamus (i.e. region 1) to the rachis tip of the feather (i.e. region 4). However, molting and inter-molting periods affect the accumulation of mercury in feathers. Large feathers molted first at the beginning of the molting process tend to exhibit more mercury than those molted later as reported elsewhere (Furness et al., 1986; Thompson et al., 1998). Our study indicate that future studies should take into account different parts of the feather, mainly the sections exhibiting the highest concentrations (e.g., feather tip) or analyze the feather as a whole to monitor mercury considering molting periods. The outcomes from the BSAF assessment portray the feasible application of this approach to derive quality standard criteria for the habitat of the Antarctic Peninsula harboring international research and military stations. For instance, the BSAF values calculated in this study can be used in conjunction with toxic effect concentration thresholds or toxicity reference values for mercury in birds reported in the literature to back calculate sediment quality guidelines-SQG (i.e. CSQG = CB/BSAF) with the aim to conserve and protect the region from potential contamination. Acknowledgements We thank the referees, Dr. W. Aguirre and Dr. J. Nieto for their review, insights and editorial work to improve the paper. Special thanks to COLACMAR and Dr. P. Muniz for the opportunity to publish this article in this special issue of the Marine Pollution Bulletin. We are in debt with the staff and military personnel of the Instituto Antartico Ecuatoriano/Ecuadorian Antarctic Institute (INAE), especially CPNV José Olmedo Morán, for the logistics and coordination for the XVI and XVII Ecuadorian-Antarctic expeditions. We thank Dr. Victoria Otton for providing valuable insights and suggestions to improve the article and we also thank Peter Olaya. This research was funded by Secretaría de Educación Superior, Ciencia, Tecnología e Innovación (SENESCYT), INAE and the Escuela Superior Politécnica del Litoral. References Anocora, S., Volpi, V., Olmastroni, S., Focardi, S., Leonzio, C., 2002. Assumption and elemation of trace elements in Adelie penguins from Antartica: A Preliminary study. Mar. Environ. Res. 54, 341–344. Alava, J.J., Ross, P.S., Lachmuth, C., Ford, J.K.B., Hickie, B.E., Gobas, Frank A.P.C., 2012. Habitat-based PCB environmental quality criteria for the protection of endangered killer whales (Orcinus orca). Environ. Sci. Technol. 46, 12655– 12663. AMAP, 2004. AMAP Assessment 2002: Heavy Metals in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo, Norway. Apperlquist, H., Asbirk, S., Drabæk, I., 1984. Mercury monitoring: mercury stability in bird feathers. Mar. Pollut. Bull. 15, 22–24. Arnot, J.A., Gobas, F.A.P.C., 2006. A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environ. Rev. 14, 257–297. Bargagli, R., Monaci, F., Sanchez-Hernandez, J.C., Cateni, D., 1998. Biomagnification of mercury in an Antarctic marine coastal food web. Mar. Ecol. Progr. Ser. 169, 65–76. Becker, P.H., González-Solís, J., Behrends, B., Croxall, J., 2002. Feather mercury levels in seabirds at South Georgia influence of trophic position, sex and age. Mar. Ecol. Progr. Ser. 243, 261–269. Bearhop, S., Phillips, R.A., Thompson Dr., Waldron, S., Furness, R.W., 2000. Bioamplification of mercury in Great Skua Catharacta skua Chicks: the
influence of trophic status as determined by stable isotope signatures of blood and feathers. Mar. Pollut. Bull. 40, 181–185. Blevin, P., Carravier, A., Jaeger, A., Chastel, O., Bustamante, P., Cherel, Y., 2013. Wide range of mercury contamination in chicks of southern ocean seabirds. PloS ONE 8, e54508. http://dx.doi.org/10.1371/journal.pone.0054508. Bond, A.L., Diamond, A.W., 2009. Total mercury concentrations in seabird feathers and eggs. Arch. Environ. Contam. Toxicol. 56, 286–291. Burger, J., 1993. Metals in avian feather: bioindicators of environmental pollution. Rev. Environ. Toxicol. 5, 203–311. Burger, J., Gochfeld, M., 2000. Metal levels in feathers of 12 species of seabirds from midway a toll in the North Pacific Ocean. Sci. Total Environ. 257, 37–52. Burger, J., Gochfeld, M., Sullvan, K., Irons, D., 2007. Mercury, arsenic, cadmium, chromium lead, and selenium in feathers of pigeon guillemots (Cepphus Columba) from Prince William Sound and the Aleutian Island of Alaska. 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Furness, R.W., Muirhead, S.J., Woodburn, M., 1986. Using bird feathers to measure mercury in the environment: relationships between mercury content and moult. Mar. Pollut. Bull. 17, 27–30. Gobas, F.A.P.C., Morrison, H.A., 2000. Bioconcentration and bioaccumulation in the aquatic environment. In: Boethling, R., Mackay, D. (Eds.), Handbook of Property Estimation Methods for Chemicals: Environmental and Health Sciences. CRC Press LLC, Boca Raton, FL, USA, pp. 189–231. Gobas, F.A.P.C., de Wolf, W., Verbruggen, E., Plotzke, K., Burkhard, L., 2009. Revisiting bioaccumulation criteria for POPs and PBT assessments. Integr. Environ. Assess. Manage. 5, 624–637. Graña Grilli, M., Montalti, D., 2012. Trophic interactions between Brown and South Polar Skuas at Deception Island, Antarctica. Polar Biol. 35, 299–304. Hughes, K., Ewins, P., Clark, K., 1997. A comparison of mercury levels in feathers and eggs of osprey (Pandion haliaetus) in the North America Great Lakes. Environ. Contam. Toxicol. 33, 441–452. Jerez, S., Motas, M., Palacios, M., Valera, F., Cuervo, J., 2011. Concentration of trace elements in feathers of three Antartic penguis: geographical and Interspecific differences. Envrion. Pollut. 159, 2412–2419. Lindberg, S., Bullock, R., Ebinghous, R., Engstrom, D., Feng, X., Fitzgerald, W., Pirrone, N., Prestbo, E., Seigneur, C., 2007. Panel on source attribution of atmospheric mercury 2007. A synthesis of progress and uncertainties in attributing the sources of mercury in deposition. Ambio 36, 19–32. Mason, R., Sheu, G., 2002. Role of the ocean in the global mercury cycle. Global Biogeochem. Cycle 16, 1–14. McArthur, T., Butler, E., Jackson, G., 2003. Mercury in the marine food chain in the Southern Ocean at Macquarie Island: an analysis of a top predator, Patagonian toothfish (Dissostichus eleginoides) and a mid trophic species, the warty squid (Moroteuthis ingens). Polar Biol. 27, 1–5. Metcheva, R., Yurukova, L., Teodorava, S., Nikolova, E., 2006. 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Mercury accumulation in sediments and seabird feathers from the Antarctic Peninsula Paola Calle a,⇑, Omar Alvarado a, Lorena Monserrate b, Juan Manuel Cevallos b, Nastenka Calle c, Juan José Alava d a
Escuela Superior Politécnica del Litoral, Facultad de Ciencias Marítimas, Oceánicas y Recursos Naturales, Guayaquil, Ecuador Escuela Superior Politécnica del Litoral, Centro de Investigaciones Biotecnológicas del Ecuador, Guayaquil, Ecuador Pacific Institute for Climate Solutions, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A1S6, Canada d School of Resource & Environment Management, Faculty of Environment, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A1S6, Canada b c
a r t i c l e
i n f o
Article history: Available online 22 November 2014 Keywords: Mercury Sediment Seabirds BMF BSAF
a b s t r a c t In an effort to assess the impact of mercury in the Antarctic Peninsula, we conducted ecotoxicological research in this region during the summer of 2012 and 2013. The objectives were to assess: (a) mercury levels in sediment samples; (b) mercury accumulation in Antarctic seabird feathers: Catharacta lonnbergi (brown skua), Pygoscelis papua (gentoo penguin) and Pygoscelis antarctica (chinstrap penguin); and (c) biomagnification (BMF predator/prey) and biota sediment accumulation (BSAF skuas/sediment) factors. Mercury concentrations in sediment were relatively low. Mercury concentrations were significantly higher in brown skuas and gentoo penguins than in chinstrap penguins (2012), and significantly higher in brown skuas than in both penguins (2013). BMF indicated 2–7.5 times greater mercury levels in brown skuas than in penguins. BSAF values suggested an apparent temporal decrease of 18.2% of this ratio from 2012 to 2013. Long-range environmental transport is the likely route of entry of mercury into the Antarctic Peninsula. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction The Antarctic continent is one of the few regions on the planet that is still considered a pristine environment; therefore, it is of particular importance to preserve this unique region. However, there are several studies that have given warning signals of possible contamination and degradation of the Antarctic environment by anthropogenic pollutants, including relatively high metal concentrations at various trophic levels of the regional marine food web (Bargagli et al., 1998; Metcheva et al., 2006; Jerez et al., 2011). Other studies have demonstrated that due to its high volatility and long residence time, mercury (Hg) can reach remote areas of the planet through long range atmospheric transport (Nriagu, 1989; Fitzgerald et al., 1998; Lindberg et al., 2007). Atmospheric Hg is predominantly the gaseous elemental form (Hg0), which can be oxidized to HgII and then deposited. It is estimated that more than 80% of the Hg deposited in the ocean is re-emitted to the atmosphere as Hg0, driving the cycle of Hg through biogeochemical reservoirs (Strode et al., 2007). The half-life of atmospheric Hg0 in polar regions is short (Driscoll et al., 2007), but ⇑ Corresponding author. E-mail address: [email protected] (P. Calle). http://dx.doi.org/10.1016/j.marpolbul.2014.10.009 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.
once Hg0 is deposited in aquatic ecosystems, it can be methylated by microorganisms to form methylmercury (Me–Hg). Me–Hg is highly toxic and bioaccumulates throughout the food web almost entirely via dietary uptake, reaching the highest concentrations in organisms at the top of the food web (Wiener et al., 2007). Seabirds have been successfully used worldwide as indicators of environmental contamination (Furness and Camphuysen, 1997; Walsh, 1990) because they exhibit different trophic levels and they have long life spans (Walsh, 1990). Seabirds can accumulate bioavailable forms of contaminants and species at high trophic levels can biomagnify contaminants to concentrations that are several orders of magnitude higher than the concentration in the environment (Burger and Gochfeld, 2000; Roomen et al., 2006). Seabird feathers have been employed as indicators of metal contamination in the environment because metals are sequestered in feathers during the birds’ growing phase (Burger, 1993) and seabirds eliminate metals through their feathers during molting (Burger, 1993: Hughes et al., 1997). In the case of Hg, the concentration of Hg in feathers has been shown to correlate with those in internal tissues (Thompson et al., 1990, 1991). Therefore, the use of feathers represents a noninvasive approach for monitoring mercury accumulation in seabirds and the marine environment (Appelquist et al., 1984; Furness et al., 1986; Thompson et al., 1990; Bond and
P. Calle et al. / Marine Pollution Bulletin 91 (2015) 410–417
Diamond, 2009). Data for mercury in seabird feathers are substantial for the North Pacific, North Atlantic and Arctic regions (Norheim, 1987; Thompson and Furness, 1989a,b; Thompson et al., 1990; Thompson et al., 1998a,b; Bearhop et al., 2000; Savinov et al., 2003; Burger et al., 2007; Bond and Diamond, 2009). Data on mercury in seabirds from the Southern Ocean and Antarctica like Antarctic penguins, brown skuas and albatrosses (Norheim et al., 1982; Thompson and Furness, 1989a,b; Ancora et al., 2002; Becker et al., 2002; Metcheva et al., 2006; Jerez et al., 2011; Blevin et al., 2013), and for seabirds from the Chilean and Argentinean coasts (Ochoa-Acuña et al., 2002; Frias et al., 2012) are gradually emerging. The aim of the present study was to assess ambient Hg levels and Hg bioaccumulation in seabirds in the Antarctic Peninsula. Specifically, this study aimed to: (a) determine concentrations of mercury in sediment and in feathers samples of the Greenwich and Barrientos Islands; and, (b) assess mercury accumulation in feathers of Antarctic seabirds, including penguins (Pygoscelis papua and P. antarctica) and brown skuas (Catharacta lonnbergi). Sampling for this study was done during the XVI and XVII EcuadorianAntarctic expeditions to Ecuador’s Scientific Station ‘‘Pedro Vicente Maldonado’’ at the Antarctic Peninsula carried out by the Ecuadorian Antarctic Institute (INAE). 2. Materials and methods 2.1. Study area The study area encompasses the Greenwich and Barrientos Islands of the Antarctic Peninsula. Greenwich Island is located at 62°310 S, 59°460 O and harbors the Ecuadorian Research Station ‘‘Pedro Vicente Maldonado’’ (i.e. Punta Fort Williams). Sampling was conducted around the station using three tracks established by the Ecuadorian Station to access the coastline of Punta Fort Williams, which enclose two sampling sites: Ensenada Guayaquil and Bahia Chile. This sector of the island is used only by the technical and military personnel that work at the Station and visiting scientists that come to the island for research purposes. Barrientos Island is located at 62°420 S, 59°470 O, and is used principally as a tourist stopover for cruise ships where tourists land and walk around the island for birdwatching. Sampling at this island was deployed around its coastline (Fig. 1). All sampling was done during the Antarctic summer and seabird breeding seasons of 2012 and 2013. A total of eleven sampling sites were surveyed for Punta Fort Williams and seven sites for Barrientos Island (Fig. 1). 2.2. Samples collection Samples of sediment were collected from eighteen locations in the Antarctic Peninsula including Ensenada Guayaquil (n = 6 sites) and Bahia Chile (n = 5 sites) of Greenwich Island and seven sampling sites of Barrientos Island (Fig. 1). Sediment samples ( 5 cm deep) were collected using a small plastic shovel and placed in Ziploc-type plastic bags. Sediment was stored at 4 °C until transportation to the laboratory in Ecuador for about one month. Once in the laboratory each sediment sample was homogenized and dried using a conventional oven at 70 °C for 48 h. Dried sediment samples (40 g) were pulverized using clean acid washed mortar and pestle. Pulverized sediment samples were stored in the desiccator until total mercury analysis. Three species of seabirds, gentoo penguins (P. papua), chinstrap penguins (P. antarctica) and brown skuas (C. lonnbergi), that inhabit the Antarctic Peninsula were identified as potential bio-indicators of Hg contamination. Hg binds strongly to the sulphydryl groups of feathers’ keratin (i.e. a high molecular weight fibrous, structural
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protein), within which organic mercury (i.e. Me–Hg) is highly stable and resistant to environment factors such as ultraviolet light, heat, freezing and weathering (Appelquist et al., 1984). Molted feathers were collected randomly in and around nests and colonies of penguins aggregated on Barrientos Island and skuas from Punta Fort Williams. While collected feathers for skuas (i.e. primary feathers) were from adult individuals, molted feathers for penguins were from chicks. Samples were brought to the laboratory of Maldonado Station and rinsed with pure acetone, followed by a generous rinse with deionized water (Burger and Gochfeld, 2000). Feathers were air dried at 20 °C, after which they were wrapped in acetone-rinsed aluminum foil and stored in the freezer (18 °C) until analysis. While the major purpose of the analysis was to measure the whole feather, we also investigated whether concentrations of Hg exhibit variation along the feather’s length. Therefore, three feathers from brown skuas (Feather 1: 33 cm; Feather 2: 22.5 cm; Feather 3: 18.0 cm) collected in 2013 where cut and analyzed in four sections from the calamus or quill (region 1) located at the base of the feather, through regions 2 and 3, to the tip of the feather rachis (region 4), as illustrated in Fig. 2. 2.3. Mercury analysis Total mercury in sediment and seabird feathers of the Antarctic Peninsula was determined via atomic absorption spectrophotometry using a Direct Mercury Analyzer (DMA-80). The advantage of using this equipment is that the instrument does not require acid digestion of the sample or other pretreatment. Because great amount of mercury in feathers is present in the form of Me–Hg, a measurement of total mercury concentration was used as a proxy of this bioavailable form (Thompson and Furness, 1989a, 1989b). The limit of detection of the equipment was 0.005 ng. Quality control and assurance was performed by analyzing the concentration of the standard reference material (SRM)-1646a Estuarine Sediment (NIST) and procedural blanks in each set of sediment and feathers samples analyzed. SRM recoveries were >94% for the 2012 samples and >93% for the 2013 samples (Table 1). For sediment samples, blanks had mean concentrations ranging from 0.0008 to 0.0015 mg/kg dw, while mean concentrations for blanks run with feathers ranged from 0.0010 to 0.0015 mg/kg dw (Table 1). All mercury concentrations are expressed as dry weight (mg/kg dw) (See Table 2). 2.4. Data treatment and statistical analysis Concentrations of mercury measured were blank-corrected using the method detection limit (i.e. MDL), defined here as the mean response of concentrations measured in n = 3 and n = 5 procedural blanks analyzed in the same run as the sediment and seabird feather samples, respectively. Most mercury concentration data were normally distributed as tested by the Shapiro–Wilk W test (p > 0.05), except for concentrations observed in skua feathers collected in 2012 and sediments from Bahia Chile collected in 2013, which were not normally distributed (Shapiro–Wilk W test, p < 0.05). Differences in contaminant concentrations among sites and seabird species were evaluated using analysis of variance (ANOVA) when variances among sites or seabird species were equal (i.e. homoscedastic as tested by the Bartlett test, p > 0.05), or Welch ANOVA when variances were unequal (i.e. heteroscedastic; Bartlett test, p < 0.05) for normally distributed data. These statistical comparisons were followed by a Tukey–Kramer honestly significant difference (HSD) multiple comparison test, which is a post hoc method recommended to test differences between pairs of means among groups that contain unequal sample sizes (Zar, 1999). Alternatively, a nonparametric test (Kruskal–Wallis test)
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P. Calle et al. / Marine Pollution Bulletin 91 (2015) 410–417
Fig. 1. Geographical location of sampling sites at the Greenwich and Barrientos Islands in the Antarctic Peninsula.
Region 1 (calamus)
Region 2
Region 3
Region 4 (rachis tip)
Fig. 2. Feather of a brown skua (C. lonnbergi) showing the subdivision of the four regions analyzed to assess the accumulation of mercury within and along the feather.
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P. Calle et al. / Marine Pollution Bulletin 91 (2015) 410–417 Table 1 Quality control and assurance measurements for analysis of reference material and procedural blanks.
a
Year
SRMa
n
Recovery% (mean ± SD)
Procedural blanks
n
Mean ± SD (mg/kg dw)
2012
Sediment Penguin Feathers Skua feathers
6 12 4
97.40 ± 2.50 94.00 ± 1.80 94.30 ± 3.60
Sediment Penguin feathers Skua feathers
18 24 9
0.0015 ± 0.0005 0.0012 ± 0.0001 0.0015 ± 0.0004
2013
Sediment Penguin Feathers Skua Feathers
6 12 4
95.50 ± 3.80 93.40 ± 1.60 94.30 ± 1.40
Sediment Penguin feathers Skua feathers
18 18 9
0.0008 ± 0.0002 0.0013 ± 0.0004 0.0010 ± 0.0001
SRM: standard reference material (SRM-1646a Estuarine Sediment, National Institute of Standardization and Technology, NIST).
for multiple comparisons was used when data did not fit a normal distribution. To determine differences in contaminant concentrations between samples collected in 2012 and 2013, either a Welch two-tailed t-test (for samples with unequal variances) or a t-test (for samples with equal variances) were used when data were normally distributed. The Wilcoxon rank-sum test was used as an alternative to the t-test when data did not follow a normal distribution. All statistical analyses were conducted using JMP 10.0 (2014 SAS Institute) at a level of significance of p < 0.05 (a = 0.05).
BMF > 1, i.e. a BMF greater than 1 indicates that the chemical is a bioaccumulative substance (Gobas et al., 2009). 2.6. Biota Sediment Accumulation Factor (BSAF) To investigate the species-habitat ecotoxicological relationship as a function of biota concentrations versus ambient concentrations (i.e. sediment or soil), the biota sediment accumulation factor (BSAF) was assessed as (Gobas and Morrison, 2000):
BSAF ¼ C B =C S
2.5. Biomagnification Factor (BMF) Because mercury biomagnification occurs in food webs, seabirds at the top of the food web are expected to accumulate higher concentrations of mercury than found in their diets or in animals at lower trophic levels. Biomagnification was expressed as the biomagnification factor (BMF) (Gobas and Morrison, 2000):
BMF ¼ C B =C D ; where CB is the concentration of mercury detected in the predator organism (i.e. brown skua) and CD is the concentration in the diet/ prey (i.e. Gentoo or chinstrap penguins). In this context, brown skuas are highly predatory seabirds feeding mainly on penguins, including eggs and mostly chicks (Reinhardt et al., 2000; Graña Grilli and Montalti, 2012), and mercury concentrations in these age categories are in turn expected to be similar to concentrations found in the parents (i.e. adult females) due to maternal transfer. Hence, the mercury levels in the feathers of penguins and brown skuas were used as surrogates for concentrations in the tissues of the whole organism, assuming that the birds had been exposed to mercury for a sufficiently long time for their Hg concentrations to reach a steady state (Gobas and Morrison, 2000). The criterion applied to indicate that mercury was biomagnified in skua was a
where CB is the chemical concentration in the predator (i.e. skua) and CS is the chemical concentration of sediment. We used mercury concentrations measured in skuas feathers and in sediments collected from Greenwich Island to determine BSAF values. A BSAF > 1 indicates the bioaccumulation potential of the chemical in relation to sediment levels (Gobas and Morrison, 2000; Arnot and Gobas, 2006). In addition, the BSAF is a bioaccumulation criterion used for ecosystem-based management purposes and as a risk assessment tool to provide potential sediment quality guidelines to protect organisms at the top of food webs (Alava et al., 2012). 3. Results 3.1. Sediments Mean concentrations of mercury ranged from 0.04 mg/kg dw in Barrientos Island to 0.06 mg/kg dw in Ensenada Guayaquil in 2012, and from 0.06 mg/kg dw in Ensenada Guayaquil to 0.20 mg/kg dw in Bahia Chile in 2013 (Fig. 3). No significant differences in total mercury sediment concentrations were found among sites in 2012 (ANOVA, df = 2, F = 1.94, p > 0.05), or among sites in 2013 (Kruskal–Wallis Test, df = 2, ChiSquare (v2) = 1.4605, p > 0.05), as
Table 2 Data for mercury concentrations in seabird feathers and sediment collected in 2012 and 2013 in the Antarctic Peninsula. Year 2012
2013
2012
2013
Sample
n
Mean ± SD (mg/kg dw)
Remarks
Seabirds: Gentoo feathers Chinstrap feathers Skua feathers
52 33 6
1.83 ± 0.80 0.83 ± 0.40 2.86 ± 2.60
Molted feathers Molted feathers Freshly fallen Feathers
Seabirds: Gentoo feathers Chinstrap feathers Skua feathers
18 18 3
0.49 ± 0.20 0.24 ± 0.01 1.80 ± 1.00
Molted feathers Molted feathers Freshly fallen Feathers
Sediment: Ensenada Guayaquil Bahia Chile Barrientos Island
6 5 7
0.060 ± 0.02 0.045 ± 0.03 0.040 ± 0.02
Surface sediment Surface sediment Surface sediment
Sediment: Ensenada Guayaquil Bahia Chile Barrientos Island
5 5 8
0.06 ± 0.02 0.20 ± 0.25 0.08 ± 0.02
Surface sediment Surface sediment Surface sediment
P. Calle et al. / Marine Pollution Bulletin 91 (2015) 410–417
shown in Fig. 2. Similarly, no temporal differences in mercury concentrations were detected in sediments collected in 2012 and 2013 (i.e. Bahia Chile: Wilcoxon test, df = 1, ChiSquare (v2) = 0.2727, p > 0.05; and, Ensenada Guayaquil, t-test, df = 9, p > 0.05) in the assessed areas, except for Barrientos Island, where mercury concentrations in sediments collected in 2013 were significantly higher than those measured in 2012 (t-test, df = 13, p < 0.05), showing a 50% increase in mean concentrations (Fig. 3).
6.00 5.00
Total Hg (mg/kg dw)
414
3.2. Seabird feathers
2012 2013
4.00
2.00
3.3. Variation in mercury concentration along the feather
A
A*
3.00
B*
1.00
Mean mercury concentrations in feathers ranged from 0.84 mg/ kg dw in chinstrap penguins to 2.90 mg/kg dw in brown skuas in the 2012 samples, and ranged between 0.20 and 1.80 mg/kg dw in chinstrap penguins and brown skuas in the 2013 samples (Fig. 4). Significant differences in total mercury concentrations were observed among feather samples collected from seabird species in 2012 (Kruskal–Wallis Test test, df = 2, ChiSquare (v2) = 16.58, p < 0.05). Mercury concentrations in chinstrap penguins (P. antarctica) feathers were significantly lower than those detected in Gentoo penguins (P. papua) and brown skuas (C. lonnbergi) (nonparametric multicomparison, Wilcoxon each pair, Z = 3.802, p < 0.05; and, Z = 2.85, p < 0.05, respectively). However, concentrations in Gentoo penguins were not significantly different from those observed in the brown skua (Wilcoxon test, Z = 0.492, p > 0.05). Similarly, significant differences in mercury concentrations were observed among feather samples collected from seabird species in 2013 (heteroscedasticity, Barlett test, p < 0.05; Welch ANOVA, p < 0.05); in the brown skua, mercury concentrations were significantly higher than the concentrations detected in Gentoo and Chinstrap penguins (Tukey–Kramer HSD test, p < 0.05), as shown in Fig. 4. Concentrations of mercury in feathers of Gentoo and chinstrap penguins collected in 2013 were significantly lower than those detected in 2012 (Gentoo: Welch t-test for unequal variances, p < 0.05; chinstrap: Welch t test for unequal variances, p < 0.05), as shown in Fig. 4. No significant differences in mercury concentrations were observed in the brown skua between 2012 and 2013 (Wilcoxon test, df = 1, ChiSquare (v2) = 0.0667, p > 0.05; Z = 0.129, p > 0.05).
A
B
B
0.00 Chinstrap pengüin
Gentoo pengüin
Brown skua
Fig. 4. Total mercury concentrations (mg/kg dw) in feathers of seabirds from the Antarctic Peninsula collected in 2012 and 2013. Concentrations in feathers not connected by the same letter differ significantly. Asterisks indicate significant differences between 2012 and 2013 for chinstrap and Gentoo penguins, respectively. Error bars are standard deviations.
feather rachis, but concentrations did not differ significantly among the regions of the feather sampled (Kruskal Wallis test, ChiSquare (v2) = 7.2051, df = 3, p > 0.05), as shown in Fig. 5. Although concentrations detected in the calamus (region 1) and regions 2 and 3 appear to be similar for all feathers (Fig. 5), high variation in mercury concentrations found in the tip (region 4) of the three feathers (i.e. mean ± SD = 3.80 ± 3.40 mg/kg dw, ranging from 1.20 mg/kg dw in feather 3 to 8.0 mg/kg dw in feather 1) may account for the lack of statistical significance. Similarly, when combining the mercury data from all regions of each feather to compare concentrations among feathers, no significant differences in mercury concentrations were observed among the three feathers of different sizes (Kruskal Wallis test, ChiSquare (v2) = 3.038, df = 2, p > 0.05), as illustrated in Fig. 6. 3.4. Mercury BMF The BMF values for the brown skua are reported in Table 3. The BMF for the brown skua/chinstrap penguin was higher than that determined for the brown skua/Gentoo penguin due to the lower concentrations of mercury observed in the chinstrap penguin relative to in the Gentoo penguins (Fig. 4). This indicates that mercury levels detected in brown skuas are 2–7.5 times greater than those found in these two species of penguins, which usually are prey for
Total mercury concentrations in brown skua feathers appear to increase from the calamus (region 1) to the tip (region 4) of the
8.00 7.00
2012 2013
Total Hg (mg/kg dw)
0.30
Total Hg (mg/kg dw)
0.25 0.20 0.15
*
0.10
6.00 5.00 4.00
Region 1 (calamus)
Region 2
Region 3
Region 4 (rachis tip)
3.00 2.00 1.00 0.00
0.05
1
2
3
4
Feather Region 0.00 Ensenada Guayaquil
Bahia Chile
Isla Barrientos
Fig. 3. Total mercury concentrations (mg/kg dw) detected in sediments collected from Barrientos Island and Greenwich Islands, Antarctic Peninsula, in 2012 and 2013. The asterisk indicates a significant difference between 2012 and 2013 for Isla Barrientos. Error bars are standard errors.
Fig. 5. Comparison and accumulation behavior of total mercury concentrations among regions of analyzed feathers (n = 3) in the brown skua. No significant differences in mercury concentrations across regions in the feathers were observed. Region 1 is the calamus at the base or lower part of the feather, while region 4 is the feather rachis tip at the top of the feather. Regions 2 and 3 are the segments found between regions 1 and 2.
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brown skuas in the region. Interestingly, an increase of about 55% in BMF values is observed from 2012 to 2013 in the study area, suggesting higher biomagnification factors in 2013 (Table 3). 3.5. Mercury BSAF The BSAF showed that mercury levels in the brown skua relative to those in sediments from Greenwich Island were 55.0–45.0 times (Table 3), and much higher compared to BMF values, indicating that concentrations of mercury in biota readily exceed ambient or abiotic (i.e. sediment) mercury concentrations and that there is a high potential transfer from sediment through the food web to apex predators. The BSAF was lower in 2013 when compared to the BSAF calculated for 2012, suggesting a temporal variability in the same area, underscoring the relatively lower concentrations of mercury found in skuas contrasting with higher mercury levels observed in sediments in 2013. 4. Discussion
Total Hg (mg/kg dw)
The lack of statistically significant differences in mercury concentrations in sediments among the sampling locations could be explained by a common global source of this pollutant. Local anthropogenic sources of mercury, which can be expected to produce differences in concentrations between human-inhabited stations (e.g., Ecuadorian Military/Navy Base, ‘‘Pedro Vicente Maldonado,’’ and several other international bases from different nations) in Greenwich Island and uninhabited islands (e.g., Barrientos Island), do not appear to be significant contributors to current sediment concentrations of mercury detected in the Antarctic Peninsula. This is further corroborated by the increase in sediment mercury concentrations found in Barrientos Island. Mercury inputs and deposition from global cycling, organic carbon content in sediments and variation in trophic transfer cannot be ruled out as factors influencing the temporal variation of mercury in biota and sediments in Barrientos Island as observed for the change in BSAF values from 2012 to 2013 (Table 3), which decreased to 70%. This appeared to be driven by higher mercury sediment concentrations in 2013 (Fig. 3) and low concentrations in skuas in the same year (Fig. 4). However, caution should be considered when interpreting this data because inter-annual variability may affect BSAFs and BMFs. Long terms studies and
Fig. 6. Box plots comparing the combined data for mercury concentrations measured in the four regions for three feathers of different lengths of the brown skua. The internal line across the middle of the box is the median; the ends of the box are the 25% and 75% quartiles; and the whisker bars are the minimum and maximum values. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Table 3 Biomagnification factor (BMF) for mercury in units of kg/kg wet weight using concentrations measured in feathers of the brown skua (predator) and two species of penguins (prey) and BSAF (skua/sediment) in units of kg/kg for Barrientos Island, Peninsula Antarctica. Year
2012 2013
BMF
BSAF
Brown skua/gentoo
Brown skua/chinstrap
Brown skua/sediment
1.60 3.60
3.40 7.50
55.0 45.0
monitoring are required to determine temporal trends in sediment and biota. The long-range transport capability of mercury species to remote areas of the world has been well documented (Fitzgerald et al., 1998; Nriagu and Pacyna, 1988; Nriagu, 1989; Mason and Sheu, 2002 AMAP, 2004; Lindberg et al., 2007; Søerensen et al., 2010). Long-range environmental transport comprising both atmospheric and oceanic processes is the likely route of entry of mercury into the marine environment of the Antarctic Peninsula and its wildlife. For instance, the short inter-temporal variation between 2012 and 2013 showed that mercury sediment concentrations in 2013 were 2.0 and 3.6 times the mercury concentrations in sediments collected in 2012 in Barrientos Island and Bahia Chile, respectively. This is of particular concern for the Antarctic environment, as mercury deposition to remote environments has increased by a factor of 3.0 since pre-industrial times (Lindberg et al., 2007). Our results show levels of mercury in penguin and skua feathers with significantly higher concentrations of mercury in gentoo penguins and brown skuas than those detected in chinstrap penguins. Metcheva et al. (2006) reported higher concentrations of several heavy metals in gentoo penguins than those detected in chinstrap penguins; however, mercury was not measured. Concentrations of mercury in chinstrap penguins were similar to previous concentrations reported for this species based on liver samples collected from specimens in Bouvetøya in the South Atlantic by Norheim et al. (1982) and Norheim (1987). Interspecific comparisons show that total mercury concentrations reported in this study for brown skuas, C. lonnbergi (2012: 2.86 ± 2.56 mg/kg dw; 2013: 1.80 ± 1.02 mg//kg dw) were lower than concentrations reported in great skua (Catharacta skua) feathers (6.34 ± 2.60 mg/kg dw) from Terra Nova Bay, Antarctica (Stewart et al., 1997). Our values are similar to concentrations reported in the Antarctic skua, Catharacta maccormicki (2.91 ± 1.93 mg/kg dw), from Shetland Islands (Bargagli et al., 1998) in Antarctica, and to that reported in one sample of the Chilean skua, Catharacta chilensis (i.e. 1.9 mg/kg dw) off the coast of Chile (Ochoa-Acuña et al., 2002). Total mercury concentrations in our seabirds were lower, comparable, and in some cases higher, relative to total mercury concentrations reported (ranging from 0.05 ± 0.01 to 5.31 ± 1.12 mg/kg dw) for 21 species of seabirds from the Subantarctic Zone (Kerguelen archipelago), Southern Ocean (Blevin et al., 2013). For instance, total mercury concentrations in our seabirds were lower than those detected in gray petrel (3.16 ± 1.21 mg/kg dw), wandering albatross (4.45 ± 1.60 mg/ kg dw), Subantarctic skua (5.15 ± 1.56 mg/kg dw) and Northern giant petrel (5.31 ± 1.12 mg/kg dw) from the Kerguelen archipelago (Blevin et al., 2013). Differences in metal concentrations in seabirds have been explained by the differences in diet and feeding habits among species (Thompson et al., 1998; Metcheva et al., 2006). Chinstrap penguin has been reported to feed exclusively on Antarctic krill, while gentoo penguin P. papua feeds on krill, fish and small squids (DelHoyo et al., 1992; McArthur et al., 2003). Methyl mercury is a highly lipophilic compound that can accumulate and biomagnify
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through the food web (Wiener et al., 2007). Prey fish are important in the transfer of MeHg to higher trophic levels (Wiener et al., 2007), which could explain the differences in Gentoo and chinstrap penguins. Biomagnification factors reported in this study indicate the mercury is been transferred from the prey to the predator (i.e. from Gentoo and chinstrap penguins to the brown skuas). While the variation in mercury concentrations within the feathers regions did not show a statistically significant increase from the calamus to the tip, there may be biological significance in terms of the tissue deposition and gradual accumulation of this metal in feathers as reflected by a relative increase in concentrations from the calamus (i.e. region 1) to the rachis tip of the feather (i.e. region 4). However, molting and inter-molting periods affect the accumulation of mercury in feathers. Large feathers molted first at the beginning of the molting process tend to exhibit more mercury than those molted later as reported elsewhere (Furness et al., 1986; Thompson et al., 1998). Our study indicate that future studies should take into account different parts of the feather, mainly the sections exhibiting the highest concentrations (e.g., feather tip) or analyze the feather as a whole to monitor mercury considering molting periods. The outcomes from the BSAF assessment portray the feasible application of this approach to derive quality standard criteria for the habitat of the Antarctic Peninsula harboring international research and military stations. For instance, the BSAF values calculated in this study can be used in conjunction with toxic effect concentration thresholds or toxicity reference values for mercury in birds reported in the literature to back calculate sediment quality guidelines-SQG (i.e. CSQG = CB/BSAF) with the aim to conserve and protect the region from potential contamination. Acknowledgements We thank the referees, Dr. W. Aguirre and Dr. J. Nieto for their review, insights and editorial work to improve the paper. Special thanks to COLACMAR and Dr. P. Muniz for the opportunity to publish this article in this special issue of the Marine Pollution Bulletin. We are in debt with the staff and military personnel of the Instituto Antartico Ecuatoriano/Ecuadorian Antarctic Institute (INAE), especially CPNV José Olmedo Morán, for the logistics and coordination for the XVI and XVII Ecuadorian-Antarctic expeditions. We thank Dr. Victoria Otton for providing valuable insights and suggestions to improve the article and we also thank Peter Olaya. This research was funded by Secretaría de Educación Superior, Ciencia, Tecnología e Innovación (SENESCYT), INAE and the Escuela Superior Politécnica del Litoral. References Anocora, S., Volpi, V., Olmastroni, S., Focardi, S., Leonzio, C., 2002. Assumption and elemation of trace elements in Adelie penguins from Antartica: A Preliminary study. Mar. Environ. Res. 54, 341–344. Alava, J.J., Ross, P.S., Lachmuth, C., Ford, J.K.B., Hickie, B.E., Gobas, Frank A.P.C., 2012. Habitat-based PCB environmental quality criteria for the protection of endangered killer whales (Orcinus orca). Environ. Sci. Technol. 46, 12655– 12663. AMAP, 2004. AMAP Assessment 2002: Heavy Metals in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo, Norway. Apperlquist, H., Asbirk, S., Drabæk, I., 1984. Mercury monitoring: mercury stability in bird feathers. Mar. Pollut. Bull. 15, 22–24. Arnot, J.A., Gobas, F.A.P.C., 2006. A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environ. Rev. 14, 257–297. Bargagli, R., Monaci, F., Sanchez-Hernandez, J.C., Cateni, D., 1998. Biomagnification of mercury in an Antarctic marine coastal food web. Mar. Ecol. Progr. Ser. 169, 65–76. Becker, P.H., González-Solís, J., Behrends, B., Croxall, J., 2002. Feather mercury levels in seabirds at South Georgia influence of trophic position, sex and age. Mar. Ecol. Progr. Ser. 243, 261–269. Bearhop, S., Phillips, R.A., Thompson Dr., Waldron, S., Furness, R.W., 2000. Bioamplification of mercury in Great Skua Catharacta skua Chicks: the
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