Transport of Nutrients and Contaminants from Ocean to Island by Emperor Penguins from Amanda Bay, East Antarctic

Science of the Total Environment 468–469 (2014) 578–583

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Science of the Total Environment

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Transport of nutrients and contaminants from ocean to island by emperor penguins from Amanda Bay, East Antarctic

Tao Huang, Liguang Sun ⁎, Yuhong Wang, Zhuding Chu, Xianyan Qin, Lianjiao Yang

Institute of Polar Environment, School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026, China

HIGHLIGHTS

• Emperor penguins transfer nutrients and contaminants from ocean to island and lake or pond system. • Stable carbon and nitrogen isotopes in determining sources of organic matters in lake sediments • Differences in biotransfer efﬁciency between emperor and Pygoscelis penguins

article info abstract

Article history: Penguins play important roles in the biogeochemical cycle between Antarctic Ocean and land ecosystems. The Received 13 June 2013 roles of emperor penguin Aptenodytes forsteri, however, are usually ignored because emperor penguin breeds Received in revised form 26 August 2013 in fast sea ice. In this study, we collected two sediment proﬁles (EPI and PI) from the N island near a large emper- Accepted 26 August 2013 or penguin colony at Amanda Bay, East Antarctic and performed stable isotope and element analyses. The organic Available online xxxx C/N ratios and carbon and nitrogen isotopes suggested an autochthonous source of organic materials for the sed- δ13 − ‰ δ15 ‰ Editor: Frank Riget iments of EPI (C/N = 10.21 ± 0.28, n =17; C= 13.48 ± 0.50 , N = 8.35 ± 0.55 , n =4)andan allochthonous source of marine-derived organic materials for the sediments of PI (C/N = 6.15 ± 0.08, 13 15 Keywords: δ C=−26.85 ± 0.11‰, δ N = 21.21 ± 2.02‰, n = 20). The concentrations of total phosphorus (TP), sele- Emperor penguin nium (Se), mercury (Hg) and zinc (Zn) in PI sediments were much higher than those in EPI, the concentration of Ornithogenic sediments copper (Cu) in PI was a little lower, and the concentration of element lead (Pb) showed no difference. As mea- Bio-transfer sured by the geoaccumulation indexes, Zn, TP, Hg and Se were from moderately to very strongly enriched in Stable isotope analysis PI, relative to local mother rock, due to the guano input from juvenile emperor penguins. Because of its high tro- Nutrients and contaminants phic level and transfer efﬁciency, emperor penguin can transport a large amount of nutrients and contaminants from ocean to land even with a relatively small population, and its roles in the biogeochemical cycle between ocean and terrestrial environment should not be ignored. © 2013 Elsevier B.V. All rights reserved.

1. Introduction penguin population (Sun et al., 2005; Wang et al., 2007). Radiocarbon dates of the ornithogenic soils/sediments and tissue remains unveiled As a typical seabird in the Southern Ocean ecosystem, penguins penguin occupation history and their relationship with regional marine are good indicator of Antarctic climate change and marine environ- environmental changes and land ice advance and retreat (e.g. Baroni ment status (Ainley, 2002; Boersma, 2008). Plentiful ecological infor- and Orombelli, 1994; Emslie et al., 2003; Huang et al., 2009b). mation could be extracted from penguin guanos and ornithogenic Seabirds transport materials from ocean to lake or pond systems in sediments to study those polar vertebrates' population records and island and coastal land by guanos, and impact the lake productivities, their responses to past climate changes and human activities (Sun the chemical compositions of lake water and sediments, and the struc- et al., 2013). For example, elemental analyses on lake sediments from ture and diversity of lake biota (e.g. Sánchez-Piñero and Polis, 2000; Ardley Island, Vestfold Hills and Ross Island identified elements such Blais et al., 2005, 2007; Ellis et al., 2006; Michelutti et al., 2009, 2011). as Sr, F, S, Se, P, Cu and Zn as geochemical markers of penguin guano in- Chemical compositions of penguin's guano reflect the status of regional puts (Sun et al., 2000; Huang et al., 2009a; Liu et al., 2013). 87Sr/86Sr ra- marine food web chemistry (Roosens et al., 2007). Antarctic land-based tios of marine-derived materials and levels of biomarker fecal sterols in penguins (Adélie, Chinstrap and Gentoo) play important roles in those lake sediments were determined and identified as good proxy for connecting ocean and land ecosystems, and they transport marine- derived nutrients and contaminants to ice free land areas in the form ⁎ Corresponding author. of guanos or dead bodies (Tatur and Mayrcha, 1984; Sun and Xie, E-mail address: [email protected] (L. Sun). 2001; Huang et al., 2011a). At Ross Island, Ardley Island and Vestfold

Hills in Antarctica, Pygoscelis penguins could transfer about 4.0 × 105 kg sea ice unstable for most of the year and provides the emperor penguin of phosphorus per year from ocean to islands and coastal lands (Qin colony in Amanda Bay with good access to the sea for feeding. Colonies et al., 2013). Pygoscelis penguins transported large amounts of marine of several thousand pairs of emperor penguins occupy variable positions heavy metals and organic pollutants from both natural and anthropo- in the southwest corner of Amanda Bay (Wienecke and Pedersen, genic sources to lands, lakes or ponds in the form of guanos, feathers 2009). and eggshells (Roosens et al., 2007; Xie and Sun, 2008; Brasso et al., During the field investigation, two sediment cores (EPI and PI) were 2012). These transported nutrients and contaminants were deposited collected at the N island, on the southwest side of the Amanda Bay in land and lakes and then formed penguin ornithogenic soils and sedi- (Fig. 1). EPI core was extracted from a pond with a 19 m height above ments. Unlike Pygoscelis penguins, emperor penguins have been less sea level while PI core was collected from a pond with a 1.5 m height studied for their roles in the biogeochemical cycle between ocean and above sea level. The PI core pond was near the emperor penguin colony land, likely due to the fact that adult emperor penguins breed in sea and many penguin feathers and even a little mummified penguin were ice and rarely visit land (Le Maho, 1977). found near the pond. In the laboratory, the cores were opened. EPI was During several field investigations, we observed many juvenile sectioned at 1 cm intervals to obtain 17 subsamples; PI was sectioned at emperor penguins in the N island near their colony, even though 0.5 cm interval on the top 4.5 cm and at 1.0 cm interval on the layer their population is smaller than that of the land-based Pygoscelis below 4.5 cm, to obtain a total of 20 subsamples. Penguin remains penguins. To study possible impacts by juvenile emperor penguins such as bones and feathers were found in PI sediment core and were on land environment, in this study, we collected two sediment handpicked. All the subsamples as well as local bedrock samples were cores (named as EPI and PI) from the N island near a large emperor stored frozen prior to analysis. penguin colony at Amanda Bay, East Antarctic and performed stable C and N isotope and elemental analyses. By comparing stable isotope 2.2. Stable isotope and elemental analysis values, elemental concentrations and sedimentary characteristic, we fi identi ed the sources of organic matters in EPI and PI, calculated the All the samples from EPI and PI were analyzed for the organic C/N geoaccumulation index of elements in PI, and discussed emperor ratio; 4 samples in EPI and 20 samples in PI were analyzed for the stable penguins' roles in transfer of nutrients and contaminants from C and N isotope ratios. Samples were air-dried, powdered, acidified with ocean to island and freshwater systems. 4 mol/l HCl of 20 ml to remove inorganic carbon, washed repeatedly with Millipore water to neutral pH, dried at 40 °C again. Samples and 2. Materials and methods standards were weighed accurately into tin capsules and loaded into element analyzer–isotope ratio mass spectrometer (Flash EA 1112 HT- 2.1. Study area and sample collection Delta V Advantages, Thermo). The instrument precision is ±0.25‰ for δ15N, ±0.20‰ for δ13C and ±0.25% for C and N content. Standard devi- Amanda Bay is located at the Ingrid Christensen Coast of Princess ation of the insert standard samples (n =5)isb0.20‰ for δ13C, b0.30‰ Elizabeth Land, East Antarctica, about 20 km northeast of Chinese for δ15N, and b0.8% and b0.7% for C and N content, respectively. Stable Zhongshan Station (Larsemann Hills) and nearly 80 km to the west of isotope results are presented in δ (‰) and expressed relative to air for Australian Davis Station (Vestfold Hills). It is approximately 3 km δ15N and Vienna Pee Dee Belemnite (VPDB) for δ13C according to the 3 wide and 6 km long, and opens northwest into the much larger Prydz equation: δ (‰) = [(Rsample − Rstandard)/Rstandard]*10 ,whereδ (‰) 15 13 Bay. The southwest side of the bay is flanked by the Flatnes Ice Tongue. represents the δ Norδ C value, Rsample is the isotopic ratio of the sam- The eastern and southern sides are bounded by the ice cliffs of the ple, and Rstandard the isotopic ratio of the air and VPDB. Hovde Glacier, with Hovde Island in the northeast. There are some For elemental analyses, about 0.25 g of sediment and bedrock pow- small islands within the bay. Fast ice within the Prydz Bay renders the der was taken, weighed, and digested (HNO3–HF–HClO4)inaTeflon

Fig. 1. Distribution of known colonies of emperor penguin in Antarctica (from Woehler, 1993) and the location of Amanda Bay in East Antarctic and the sampling sites EPI and PI in this study. 580 T. Huang et al. / Science of the Total Environment 468–469 (2014) 578–583 crucible with electric heating. The digested samples were analyzed for TP, Cu, Zn and Pb by inductively coupled plasma-optical emission spec- troscopy (ICP-OES, Perkin Elmer DV2100) and for Hg and Se by atomic ﬂuorescence spectrophotometry (AFS-930, Titan Instruments Co., Ltd.). Standard sediment reference materials were included with every batch of samples. The analytical values for major elements and trace elements were within ±0.5% and ±5% of the certiﬁed standards, respectively. According to the equation given by Müller (1979) (Igeo =log2 [Cn/1.5Bn]), the geoaccumulation index of 6 elements in PI sediment was calculated, where Cn represents the elemental concentrations in PI sediments, Bn the elemental concentrations in local bedrock, and 1.5 is a correction factor.

2.3. Statistical test for isotopic and elemental data between PI and EPI

To assess the signiﬁcance of the difference in stable isotope ratios (δ13Candδ15N, n = 20 for PI and n = 4 for EPI) and elemental concentrations (C/N, TP, Cu, Zn, Hg, Se and Pb, n = 20 for PI and n =17for EPI) between PI and EPI, we performed two-step statistical tests by using SPSS 16.0. First, we performed the nonparametric one-sample Kolmogorov–Smirnov test to verify if the data follow normal distribution. The results showed that all of our data in PI and EPI follow normal distribution (asymptotic p value N 0.10 with no presence of ties). Sec- ond, we performed parametric independent samples t-test and used 0.05 for the level of signiﬁcance.

3. Results

Fig. 2. Isotope values vs. C/N ratios in EPI and PI. a: δ13C, b: δ15N, triangle for PI, and dot for 3.1. C/N ratios and stable isotopes EPI.

The C/N ratios of the PI sediments range from 5.38% to 6.66% with a mean of 6.15 ± 0.08% (mean ± standard error of mean, n =20).The C/N ratios of the EPI sediments range from 9.83% to 11.82% with a mean 4. Discussion of 10.21 ± 0.28% (n = 17). There is a significant difference in the C/N ratios of sediments between PI and EPI (t = 6.984, p =0.005).Theδ13C 4.1. Sources of organic matter in PI and EPI values in the PI sediments range from −25.76‰ to −27.35‰ with a mean of −26.85 ± 0.11‰ (n = 20); the δ15N values have a greater The ecosystem of Antarctic islands and coastal ice free land areas is range from 15.05‰ to 47.09‰ with a mean of 21.21 ± 2.02‰ relatively simple. The organic matters in Antarctic lake or pond sedi- (n =20).Theδ13C values in the EPI sediments range from −12.05‰ ments are mainly from autochthonous algae or allochthonous floras to −14.29‰ with a mean of −13.48 ± 0.50‰ (n =4);theδ15N values and faunas (e.g. Sun et al., 2013). During the core section, visual inspec- range from 6.98‰ to 9.64‰ with a mean of 8.35 ± 0.55‰ (n = 4). Sta- tion showed a homogenous lithostratigraphy for EPI and PI cores. EPI is ble C and N isotope values between PI and EPI show a significant differ- composed of mainly peat and PI of mainly black mud with a strong un- ence (δ13C: t =26.202, p b 0.001; δ15N: t = 6.139, p b 0.001), and pleasant smell of penguin guano. Mean C/N ratios of PI and EPI (6.15 ± they are plotted vs.C/NratiosintheFig. 2. 0.08% and 10.21 ± 0.28%) are within the range of 4%–10% (Fig. 2), indicating a lacustrine or marine organic sedimentation (Meyers, 1994). PI has C/N ratios closer to those of sedimentary organic matters from

3.2. Elemental concentrations and geoaccumulation index (Igeo) Southern Ocean (mean: 6.2 ± 0.5%, range: 5.0%–6.9%, n =11,data from Sigman et al., 1999) than EPI. Though the difference in C/N ratios The mean concentrations of TP, Hg, Se, Zn, Cu and Pb in sedi- between PI and EPI sediments is significant, we cannot distinguish ments of PI are 2.5 ± 0.3%, 281 ± 25 ng g−1, 9.1 ± 1.1 mg kg−1, their exact original sources since the C/N ratios in PI and EPI are within 652 ± 86 mg kg−1, 22.3±2.1mgkg−1 and 23.8 ± 1.7 mg kg−1, the range of both lacustrine and marine organic materials. respectively. The mean levels of corresponding elements in EPI δ13C is a useful proxy in tracing organic sources in sediments (Meyers, are 0.29 ± 0.01%, 55.5 ± 2.1 ng g−1,2.9±0.2mgkg−1,138± 1994). The δ13C values of lake algae are usually around −27‰ (Meyers, 19 mg kg−1,35.3±3.1mgkg−1 and 20.5 ± 1.3 mg kg−1,respec- 1994), but they can increase to reach as high as −9‰ when the algae tively. Elemental concentrations vs. C/N ratios in PI and EPI are plotted begin to use dissolved bicarbonate as the carbon source (Meyers, 2003). in Fig. 3. PI has higher levels of TP, Hg, Se and Zn and lower levels of Marine phytoplankton typically has δ13C values between −22‰ and Cu than EPI, and the differences are significant for TP, Hg, Se, Zn and −20‰, and the δ13C values of particulate organic carbon in Southern Cu (TP: t =6.411,p b 0.001; Hg: t = 8.231, p b 0.001; Se: t = 4.979, Ocean are around −26‰ (Berg et al., 2011). The mean δ13C value of p b 0.001, Zn: t =5.377, p b 0.001, Cu: t = 3.485, p =0.002)and −13.48 ± 0.50‰ in the EPI sediments indicates freshwater algae insignificant for Pb (t = 1.464, p = 0.152). sedimentation, and this is further supported by the observed sedi- 13 The geoaccumulation indexes (Igeo) of 6 elements in PI are shown in mentary characteristic. High δ C values in lake sediments are also Fig. 4. TP, Hg, Se and Zn have high Igeo values with a mean of 2.8 ± 0.2, observed in the nearby Larsemann Hills (mean: −9.90‰, range: 2.9 ± 0.1, 5.6 ± 0.2 and 1.2 ± 0.2, respectively; Cu and Pb have nega- −11.31‰–−8.92‰, n = 63, Liu et al., unpublished results). 13 tive Igeo values. These high δ C values of lake sediments in East Antarctica suggest T. Huang et al. / Science of the Total Environment 468–469 (2014) 578–583 581

Fig. 3. Elemental concentrations vs. C/N ratios in the sediments of PI and EPI. Triangle is for PI, and dot for EPI. that lake algae use bicarbonate as carbon sources. The δ13Cvalues original organic sources. Since the freshwater algae sedimentations in of the PI sediments range from −25.76‰ to −27.35‰ with a both the N island (EPI) and the nearby Larsemann Hills have high δ13C mean of −26.85 ± 0.11‰, indicating either freshwater or marine values, the distinctly low δ13C values in PI suggest a marine source of its organic matters. Average δ13C values of Pygoscelis penguin ornithogenic sediments from Ardley Island and Ross Island in Antarctica are −22.61‰ (n = 12) and −24.06‰ (n = 116), respectively (Liu et al., 2006, 2013); and they are very close to the values of PI sediments, a further indication of the marine source of the organic matters in PI. In contrast to carbon isotope ratio (δ13C), stable nitrogen isotope ratio (δ15N) is much enriched in consumers relative to that of prey and consequently it usually serves as indicator of a consumer trophic position (e.g. Emslie and Patterson, 2007; Huang et al., 2011b). The mean δ15N value in the PI sediments is 21.21 ± 2.02‰, much higher than that of EPI (8.35 ± 0.55‰). According to the local sedimentary environment, PI should be ornithogenic sediments as the result of juvenile emperor penguins' guano input. The high δ15N values in PI are very likely due to substantial fractionation in the penguin guanos from ammonia volatilization, during which lighter nitrogen-14 is emitted with ammo-

Fig. 4. Geoaccumulation index of elements in the PI sediments (data was presented by nia and heavier nitrogen-15 is enriched in the remaining sediments. mean ± standard error of mean, n = 20). Similarly high nitrogen isotopic ratios are observed in Adélie penguin 582 T. Huang et al. / Science of the Total Environment 468–469 (2014) 578–583 ornithogenic soils (32.2‰, n =6,Mizutani et al., 1986), Adélie penguin Island (150 ± 8 ng g−1, n =3)(Nie et al., 2012). The great differences guanos (25.0‰, n = 3), ornithogenic sediments (28.4‰, n = 11, Huang in Hg concentration between Adélie and emperor penguin ornithogenic et al. unpublished results), and seal excrement sediments (24.0‰, n = sediments are mainly due to their different trophic positions. Unlike 32, Liu et al., 2004). By comparing stable C and N isotope values of PI Adélie penguins, which mainly feed on krill of lower trophic level, em- and EPI, we conclude that PI sediments are affected by emperor peror penguins eat fishes of higher trophic level and occupy a higher penguin's guano input while EPI sediments are from natural lake trophic position (Cherel, 2008). Because of their high transfer efficiency, algae sedimentation. emperor penguins' role in transferring materials from ocean to land should not be underestimated or even ignored, especially in the barren 4.2. Emperor penguins transfer nutrients and contaminants from ocean to Antarctic terrestrial systems, even though the population of juvenile island emperor penguins that visited on land is smaller than that of Adélie penguins. The transport of large amount of nutrients and contaminants from ocean to the Antarctic islands and coastal ice free land areas by the 5. Conclusion land-based Pygoscelis penguins have been studied (e.g. Sun and Xie, ę 2001; Roosens et al., 2007; N dzarek, 2010). Emperor penguins' role Based on stable isotope and elemental geochemical analyses on in such transport, however, is usually ignored because they are sea ice two sediment cores EPI and PI from the N island near Amanda Bay, breeding species (Le Maho, 1977). Our stable isotope analyses suggest we conclude that EPI is composed of natural freshwater algae sedi- natural lacustrine algae sedimentation in EPI and marine-derived em- mentation and PI is strongly influenced by emperor penguin guano peror penguin guano deposition in PI. The concentrations of TP, Hg, Se, input. The Igeo values of elements in PI sediments show that emperor and Zn in ornithogenic sediments of PI are much higher than those of penguins at Amanda Bay have significant impacts on local island and EPI, the concentration of Cu is a little lower, and Pb shows no difference. pond systems. Juvenile emperor penguins transfer large amounts of Thus, Cu and Pb mainly originate from local mother rock and are not af- nutrients and contaminants from Southern Ocean to island environment, fected by penguin guano input. and lead to substantial enrichment of Se, TP and Hg in lake sediments. The geoaccumulation index (Igeo)byMüller (1979) has been exten- Though the population of emperor penguins that have direct impacts sively used for evaluating contamination and enrichment of elements in on land systems is small, emperor penguins' role in the biogeochemical fi sediments. Förstner et al. (1993) classi ed sediments into seven classes cycle between ocean and land should not be ignored, especially in the b based upon Igeo, from practically unpolluted level (class 0, Igeo 0) to Antarctic land systems. very strong pollution level (class 6, Igeo N 5). The Igeo of elements in PI are plotted in Fig. 4. Nutrient element Se has the highest I value of geo fl 5.6 ± 0.8, indicating a very strong enrichment, apparently because of Con ict of interest the very high concentration of Se in emperor penguin ornithogenic sed- fl iments and the very low level in local mother rock. High concentration The authors declare no con ict of interests. of Se in Pygoscelis penguin guanos and ornithogenic sediments from Ardley Island, Victoria Land and Vestfold Hills in Antarctica was also ob- Acknowledgments served (Sun et al., 2000; Hofstee et al., 2006; Huang et al., 2009a). The

Igeo of nutrient element TP and pollution element Hg in PI are 2.8 ± This study was funded by NSFC (Nos. 41106162 and 40730107), Chinese 0.2 and 2.9 ± 0.1, indicating moderate to strong enrichment and pollu- Polar Environment Comprehensive Investigation & Assessment Programmes tion of them, apparently due to penguin guano input. The Igeo of heavy (CHINARE2013-02-01-03, CHINARE2013-04-01-07 and CHINARE2013-04- metal of Zn in PI is 1.2 ± 0.2, a moderately pollution level. The Igeo of 04-09) and the Central Universities (WK2080000017). Samples in this study Cu and Pb in PI are negative, indicating that Cu and Pb are not affected were provided by the BIRDS-Sediment system. We thank the Chinese Arctic by penguin guano input. Different homeostatic processes from non- and Antarctic Administration and Polar Research Institute of China for logistical essential elements Hg and Pb in contrast to essential elements TP, Se, support in field; Dr. Jie Tang and Changgui Lu provide help in field for samples Cu and Zn may cause a bias in our dataset. However, the non-essential collection. element Hg has an Igeo value comparable to that of the essential element TP and Pb has much lower value of I than TP and Hg; thus the effects geo References of the homeostatic processes of elements on the dataset in the present study are likely insignificant. The geoaccumulation index values of ele- Ainley DG. The Adélie penguin: bellwether of climate change. New York: Columbia Uni- ments in PI and EPI showed that juvenile emperor penguins transferred versity Press; 2002. Baroni C, Orombelli G. Abandoned penguin rookeries as Holocene paleoclimatic indicators a large number of nutrients and contaminants from ocean to island in Antarctica. Geology 1994;22:23–6. system. Berg GM, Mills MM, Long MC, Bellerby R, Strass V, Savoye N, et al. Variation in particulate Trophic position of seabirds influences their efficacy in transfer- C and N isotope composition following iron fertilization in two successive phytoplankton communities in the Southern Ocean. Global Biogeochem Cycles 2011;25: ring pollutants from ocean to land. Seabirds of higher trophic posi- GB3013. tion are more efficient transferer (Michelutti et al., 2010)because Blais JM, Kimpe LE, McMahon D, Keatley BE, Mallory ML, Douglas MSV, et al. Arctic sea- many pollutants become biomagnified through food webs. Pb level birds transport marine-derived contaminants. Science 2005;309:445-445. Blais JM, Macdonald RW, Mackey D, Webster E, Harvey C, Smol JP. Biologically mediated does not show any substantial difference between emperor penguin transport of contaminants to aquatic systems. Environ Sci Technol 2007;4:1075–84. ornithogenic sediments PI and Pygoscelis penguin ornithogenic sed- Boersma PD. Penguins as marine sentinels. Bioscience 2008;58:597–607. iments Y2 (23.8 ± 1.7 mg kg−1 vs.15.7±0.7mgkg−1, data from Brasso RL, Polito MJ, Lynch HJ, Naveen R, Emslie SD. Penguin eggshell membranes reflect this study and Sun and Xie, 2001), mainly because Pb is not homogeneity of mercury in the marine food web surrounding the Antarctic Peninsula. Sci Total Environ 2012;439:165–71. bioaccumulated through food chain (Sun and Xie, 2001). The concen- Cherel Y. Isotopic niches of emperor and Adélie penguins in Adélie Land, Antarctica. Mar tration of Hg, however, increases in living organisms along the trophic Biol 2008;154:813–21. fi Ellis JC, Fariña JM, Witman JD. Nutrient transfer from sea to land: the case of gulls and cor- chain through bioaccumulation and biomagni cation (Riisgard and – −1 morants in the Gulf of Maine. J Anim Ecol 2006;75:565 74. Hansen, 1990). The Hg level in PI is as high as 281 ± 25 ng g , Emslie SD, Patterson WP. Abrupt recent shift in delta C-13 and delta N-15 values in Adélie much higher than those in Adélie penguin ornithogenic sediments penguin eggshell in Antarctica. Proc Natl Acad Sci U S A 2007;104:11666–9. from Ardley Island and Vestfold Hills (55 ± 2 ng g−1 (n = 46) and Emslie SD, Berkman PA, Ainley DG, Coats L, Polito M. Late-Holocene initiation of ice-free – −1 ecosystems in the southern Ross Sea, Antarctica. Mar Ecol Prog Ser 2003;262:19 25. 10 ± 0.4 ng g (n = 55), respectively) (Sun et al., 2006; Huang Förstner U, Ahlf W, Calmano W. Sediment quality objectives and criteria development in et al., 2009a) and even those in pure Adélie penguin guanos from Ross Germany. Water Sci Technol 1993;28:307–14. T. Huang et al. / Science of the Total Environment 468–469 (2014) 578–583 583

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