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Geochemical record of high emperor penguin populations during the Little Ice Age at Amanda Bay, Antarctica
Science of the Total Environment 565 (2016) 1185–1191
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Geochemical record of high emperor penguin populations during the Little Ice Age at Amanda Bay, Antarctica Tao Huang a,b,⁎, Lianjiao Yang b, Zhuding Chu b, Liguang Sun b,⁎⁎, Xijie Yin c a b c
School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026, China Third Institute of Oceanography, State Oceanic Administration, Xiamen 361005, China
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Emperor penguin colonized at Amanda Bay, East Antarctic as early as AD 1540. • Populations of emperor penguin at Amanda Bay increase during the little ice age. • Depleted N isotope ratios of Emperor penguins during the LIA were observed.
a r t i c l e
i n f o
Article history: Received 25 March 2016 Received in revised form 19 May 2016 Accepted 23 May 2016 Available online 31 May 2016 Editor: F. Riget Keywords: Emperor penguin Stable isotope analysis Bio-elements Little Ice Age Foraging habitat Sea ice
a b s t r a c t Emperor penguins (Aptenodytes forsteri) are sensitive to the Antarctic climate change because they breed on the fast sea ice. Studies of paleohistory for the emperor penguin are rare, due to the lack of archives on land. In this study, we obtained an emperor penguin ornithogenic sediment profile (PI) and performed geochronological, geochemical and stable isotope analyses on the sediments and feather remains. Two radiocarbon dates of penguin feathers in PI indicate that emperor penguins colonized Amanda Bay as early as CE 1540. By using the bio-elements (P, Se, Hg, Zn and Cd) in sediments and stable isotope values (δ15N and δ13C) in feathers, we inferred relative population size and dietary change of emperor penguins during the period of CE 1540–2008, respectively. An increase in population size with depleted N isotope ratios for emperor penguins on N island at Amanda Bay during the Little Ice Age (CE 1540–1866) was observed, suggesting that cold climate affected the penguin's breeding habitat, prey availability and thus their population and dietary composition. © 2016 Elsevier B.V. All rights reserved.
⁎ Correspondence to: T. Huang, School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China. ⁎⁎ Corresponding author. E-mail addresses: [email protected] (T. Huang), [email protected] (L. Sun).
http://dx.doi.org/10.1016/j.scitotenv.2016.05.166 0048-9697/© 2016 Elsevier B.V. All rights reserved.
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1. Introduction The emperor penguin (Aptenodytes forsteri) is known to be extremely sensitive to changes in climate and sea ice dynamics. Recent model studies have estimated that at least two-thirds of emperor penguin colonies will have dramatically declined by more than half at the end of this century if sea ice extent decrease at the rate predicted by the Intergovernmental Panel on Climate Change (IPCC) (Jenouvrier et al., 2009; Ainley et al., 2010). Since it breeds on the fast sea ice and feeds only at sea, its population size and foraging behavior are affected dominantly by marine environmental variability. For example, census data from Terre Adélie show that the emperor penguins have declined by N50% during the late 1970s when there was an abnormally warm period with reduced sea-ice extent (Barbraud and Weimerskirch, 2001). Since 1902 when the first breeding colony was discovered (Wilson, 1907), many studies using the methods of ground counts, aerial photos and remote sensing have provided more and more information on the populations, colonies and foraging habitat of emperor penguin around the Antarctic continent (e.g. Robertson, 1992; Cherel and Kooyman, 1998; Barber-Meyer et al., 2007; Wienecke and Pedersen, 2009; Fretwell and Trathan, 2009; Wienecke, 2010; Trathan et al., 2011; Fretwell et al., 2012, 2014). Unlike Pygoscelis penguins which have left an extensive records of their occupation history, population size and dietary change in the ornithogenic soils and sediments (e.g. Sun et al., 2000, 2013; Emslie and Patterson, 2007, Emslie et al., 2014), the emperor penguins have been less studied for their paleohistory due to the lack of archives on land because most of their remains are lost to the ocean when the sea ice melts in summer. Using mitochondrial DNA from modern colonies and sub-fossil remains, Younger et al. present that emperor penguin population expanded several-fold during the Holocene from the Last Glacial Maximum (LGM), which suggests an optimal sea ice condition occur for this species, corresponding to accessible foraging habitat (Younger et al., 2015, 2016a, 2016b). These genetic studies investigated how emperor penguin populations were affected by climate changes during and following the LGM, though the resolution is relative low over shorter timescales. During field investigations, we observed
many emperor penguins on an island around Amanda Bay, East Antarctic. Those emperor penguins have transferred a large amount of nutrients and contaminants from ocean to land and formed penguin ornithogenic sediments (Huang et al., 2014a). In this study we collect a penguin ornithogenic sediment core (PI) at Amanda Bay, establish its chronology by radiometric and radiocarbon dating, and reconstruct the population size and dietary changes of visited emperor penguins by geochemical markers (bio-elements and stable isotopes) in PI sediments and organic remains.
2. Materials and methods 2.1. Sample collection and chronology The penguin ornithogenic sediment core was collected at the N island, on the southwest side of the Amanda Bay, Ingrid Christensen Coast of Princess Elizabeth Land, East Antarctica (Fig. 1) in 2008. During the field season, a 9-cm diameter PVC pipe was pushed vertically into the centre of the pond to collect a core and named it as PI. In the laboratory, this 14-cm-long core was sectioned at 0.5 cm intervals on the top 4.5 cm and 1.0 cm below 4.5 cm, to obtain a total of 20 subsamples. Penguin remains such as feathers and bones were picked from each subsample. Before chemical analyses, each subsample was air-dried in a clean laboratory and homogenized. To establish the chronology of PI, we performed radiometric dating (210Pb, 137Cs) and AMS14C dating. 210Pb, 226Ra and 137Cs dating was performed on each subsample by direct gamma spectrometry using an Ortec HPGe GWL series detector. In addition, two feather samples from the bottom of PI (13 and 14 cm depths) were dated by AMS14C analysis at W.M. Keck Carbon Cycle Accelerator Mass Spectrometry Laboratory, University of California Irvine. The conventional radiocarbon dates were corrected and calibrated using the CALIB 5.1.0 program (Stuiver et al., 2005) and the dataset of Marine04 (Hughen et al., 2004), with a marine reservoir effect (ΔR) of 1700 years. This ΔR was selected based on the fact that modern marine algae have a 14C age of 1700 years in East Antarctic ocean (Domack et al., 1991).
Fig. 1. Study area and the sampling site PI near Amanda Bay, East Antarctic.
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2.2. Elemental and stable isotope analyses The concentrations of element P, Cu, Zn, Pb, Hg and Se, stable carbon and nitrogen isotope values as well as the ratios of C/N in the sediments of PI were analyzed and published in Huang et al. (2014a). In this study, the concentration of Cd in PI sediments was analyzed by using the same method in Huang et al. (2014a). Contents of Total Carbon (TC), Total Nitrogen (TN), Total Sulfur (TS) and Total Hydrogen (TH) were measured by vario EL III (Elementar, Germany) with a relative error of 0.1%. Twenty feather samples picked from each subsample of PI were analyzed for the stable C and N isotopes as well as C/N ratios. Samples were cleaned with Millipore water and 2:1 chloroform: methanol solution, and then dried at 40 °C. Samples and standards were weighed accurately into tin capsules and loaded into element analyzer-isotope ratio mass spectrometer (Flash EA1112 HT- 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 deviation of the insert standard samples (n = 5) is b0.25‰ for δ13C, b 0.20‰ for δ15N, and b0.2% and b0.2% for C and N content, respectively. Stable isotope results are presented in δ (‰) and expressed relative to air for δ15N and Vienna Pee Dee Belemnite (VPDB) for δ13C according to the equation: δ (‰) = [(Rsample − Rstandard)/Rstandard] ∗ 103, where δ (‰) represents the δ15N or δ13C value, Rsample is the isotopic ratio of the sample, and Rstandard the isotopic ratio of the air and VPDB. 2.3. Statistical test for isotopic and elemental data in PI
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sediments of PI are 15.5 ± 1.6% (mean ± standard error of mean, 5.4%–30.7%, n = 20), 2.7 ± 0.3% (0.8–6.0%, n = 20), 0.6 ± 0.1% (0.2%– 1.2%, n = 20) and 2.0 ± 0.3% (0.2%–4.4%, n = 20), respectively. TC, TN and TH show similar decreasing trend from bottom to top in the profile. The data of TC/TN, δ15N and δ13C in sediments suggested a source of penguin-derived organic materials for PI (Huang et al., 2014a). Geochronological results for PI are shown in Fig. 3 and Table 1. The activity of 210Pb in PI displayed a down trend with fluctuations against depth, while that of 226Ra was increasing in the top 2 cm and then decreasing gradually (Fig. 3a). They came to equilibration at 9.0 cm, indicating the decreasing excess 210Pb reached its zero point. A CRS (Constant Rate of Supply) model was used for 210Pb dating calculation (Appleby, 2001) and PI was dated back to CE 1827 at the depth of 9.0 cm. The signal of 137Cs in PI was weak and showed a decreasing trend with two peaks at the surface and the depth of 2.0 cm, respectively. The later might be corresponding to the Chernobyl nuclear accident in 1986. However, there is no signature for the bomb testing in 1960s. In addition, two radiocarbon results are shown in Table 1. The mean calibrated ages of penguin feathers at 13 and 14 cm are about CE 1624 and 1540, respectively. The chronology of PI was established using polynomial interpolation by these two 14C dates and the 210Pb dates in the top 9.0 cm which were fitted well in the regression line (Fig. 3b). 3.2. Elemental concentrations in PI sediments
We ran Pearson correlation analysis on concentrations of elements and TC, TN, TS, TH using SPSS16.0, to examine the relationship between elements and TC, TN, TS, TH in the sediments. To assess the significance of the difference in stable isotope ratios between different periods, we performed two-step statistical tests in 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 the stable isotope data in PI follow normal distribution. Second, we performed parametric independent samples t-test and used 0.05 for the level of significance.
The concentration data of phosphorus (P), selenium (Se), mercury (Hg), copper (Cu), zinc (Zn) and lead (Pb) in PI sediments were published in Huang et al. (2014a). The mean concentration of cadmium (Cd) in sediments of PI is 3.0 ± 0.3 mg kg−1 (1.0–5.7 mg kg− 1, n = 20). Overall, the elements P, Se, Hg, Cu, Zn and Cd show a very similar decreasing trend from bottom to top in their profile, with a higher level at the depth of 8.5–14 cm and low between 8.0 and 0 cm (Fig. 4). Element of Pb, however, shows an opposite vertical trend in comparison with those of other 6 elements. Pearson correlation analyses on these elements and TC, TN, TS and TH were performed and the results are listed in Table 2. P, Se, Hg, Cu, Zn, Cd, TC, TN and TH are significantly correlated with each other and they are negatively correlated with Pb.
3. Results
3.3. Stable isotope values in penguin feathers
3.1. Sedimentology and chronology
The C/N ratios of the penguin feathers in PI range from 3.03% to 3.39% with a mean of 3.17 ± 0.02% (n = 20); they remain stable in the studied time period (Fig 4), indicating a good preservation of the penguin feathers. The δ13C values in the penguin feathers range from − 21.32‰ to − 23.88‰ with a mean of − 22.86 ± 0.16‰ (n = 20); the δ15N values have a greater range from 11.68‰ to 19.18‰ with a mean of 14.85 ± 0.42‰ (n = 20). For the overall profile, the δ15N values show an increasing trend over time, while δ13C values do not. Depleted
PI is a 14-cm-long core with a homogeneous sedimentary characteristic (Fig. 2). It consists of olive to dark olive clay with many physical penguin remains such as bones and feathers, and has a strong smell of penguin guano. PI was identified as an ornithogenic sediment profile by the sedimentary characteristic and geochemical compositions in sediments (Huang et al., 2014a). The total contents of C, N, S and H in
Fig. 2. The sedimentology and concentration profiles of TC, TN, S, TH, δ15N, δ13C and TC/TN in PI sediments.
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Fig. 3. Geochronological results of PI. a: Activity of radionuclides measured in the PI sediments. b: the age profile of PI based on the 210Pb and 14C dates.
penguin N isotope ratios (13.45 ± 0.55, n = 7) occurred from CE 1540 to 1866 during the Little Ice Age (LIA), while high N isotope values (15.60 ± 0.46, n = 13) of penguins between CE 1866–2008. Emperor penguins show a significant difference (t = 2.879, p = 0.01) in their N isotope values between CE 1540–1866 and 1866–2008. 4. Discussion
here to track activities of emperor penguin populations. Therefore, concentrations of these bio-elements in PI are considered to be geochemical markers for changes in emperor penguin guano inputs and thus penguin population size around the pond catchment. Specifically, high concentration of bio-elements indicates high level guano inputs and thus greater penguin numbers. The level of bio-elements in PI indicates high emperor penguin population size during the year of CE 1540–1866, and low between CE 1891–2008 in N island, Amanda Bay (Fig. 4). It should be noted that the inferred high emperor penguin population size during CE 1540– 1866 corresponds to a recent neoglacial episode or Little Ice Age (CE 1450–1850) as recorded in an ice core from the Princess Elizabeth Land, East Antarctica (Li et al., 2009). Such association may be explained by the impacts of climate-related changes on this sea-ice breeding species. During the period of neoglacial climates, extended sea ice cover provides ample nesting and breeding sites for emperor penguins. This change is opposite to that of Adélie penguins on Vestfold Hills which decreased in population size during the Little Ice Age (Huang et al., 2011a), as more snow or ice cover on land during cold climate making it harder for the land breeding Adélie penguins to nest and breed. It should be noted that the effective emperor population sizes are smaller during the LGM which is likely due to the severely restricted foraging habitat available for penguins (Younger et al., 2015, 2016a). In this study, the geochemical evidence of high penguin populations during the LIA implies an unrestricted access to foraging area for emperor penguins at that time period. This is likely because the climate during the LIA in Antarctica is mild in contrast to that in northern hemisphere (Bertler et al., 2011). Indeed, it has been proposed that there is an optimal sea ice condition at the large spatio-temporal scale for emperor penguins, corresponding to ample breeding sites and available foraging area (Ainley et al., 2010; Younger et al., 2015). The inferred emperor penguin populations declined from CE 1978 (Fig. 4), similar to that decrease in the observational emperor penguin populations in Terre Adélie Land, East Antarctica during the late 1970s when there was an abnormally warm period with reduced sea-ice extent (Barbraud and Weimerskirch, 2001).
4.1. Bio-elements as geochemical markers for emperor penguin populations 4.2. Dietary change of emperor penguins from feather isotopic signature Many elements are enriched in seabird guanos, ornithogenic soils and sediments, and they are considered as bio-elements and indicators of sources from seabird activities (Sun and Xie, 2001, Sun et al., 2013; Blais et al., 2007; Emslie et al., 2014). In Antarctica for Pygoscelis penguin species, these reported bio-elements include F, P, S, Se, Cu, Zn, Ca, Sr, Be, As, Fe, Mg and Mn in Ardley Island and King George Island, South Shetland Islands (Sun et al., 2000; Zdanowski et al., 2005; Xie and Sun, 2008), F, P, S, Se, Cu, Sr, Cd, Mg and As in Vestfold hills (Huang et al., 2009, 2011a), and F, P, S, Mg, Ca, Hg, Se, As, Cu, Zn, and Cd in Ross Island and Victoria Land along the Ross Sea (Hofstee et al., 2006; Liu et al., 2013; Nie et al., 2015). Our geochemical analyses on PI sediments and local mother rock indicated that elements P, Hg, Se, Zn and Cd are enriched in emperor penguin ornithogenic sediments, with the high Igeo values (geoaccumulation indexes) of 2.8, 2.9, 5.6 and 1.2 for P, Hg, Se and Zn, respectively (Huang et al., 2014a). The Igeo of Cd was not calculated since its very low level in mother rock which is below the detection limit of the analytical techniques. These marine-derived elements are transported to terrestrial environment by penguins in the form of guanos and/or dead bodies, and thus they are defined as bio-elements
Stable carbon and nitrogen isotope ratios in tissues have been used extensively in tracing marine animal foraging habitats, trophic level or diets and migration patterns (Cherel and Hobson, 2007; Newsome et al., 2010; Huang et al., 2011b, 2014b). This is based on the fact that in marine environments, the stable nitrogen isotope ratio (15N/14N, δ15N) shows an enrichment of ~ 3‰–5‰ from prey to consumer, and it could therefore be used as an indicator for the diet and trophic level of marine predators (Hobson et al., 1994). In contrast, the carbon isotope ratio (13C/12C, δ13C) vary little through the marine food chain (b 1‰) but changes remarkably between habitats. For example, δ13C signature of particulate organic matter increases from offshore to inshore waters (Trull and Armand, 2001), and δ13C could serves as a carbon source tracer and provide information on the foraging habitat of the studied consumers (Cherel et al., 2011). Stable isotopes in tissues have different turnover rates and time scales, from days for blood, to weeks for feathers (Bearhop et al., 2003). Carbon and nitrogen isotopic signatures in penguin feathers reflect those of the average diets at the time of feather growth.
Table 1 14 C dates and calibrated ages using CALIB 5.1.0 and the Marine04 datasets (ΔR: 1700 ± 30). Calibrated age (CE) UCIAMS number
Sample number
Sample material
Depth (cm)
Conventional
55720 55719
PI-19 PI-20
Feather Feather
13 14
2410 ± 15 2445 ± 15
14
C age (yr BP)
Note: The dates are measured at the W.M. Keck Carbon Cycle Accelerator Mass Spectrometry Laboratory, University of California Irvine (KCCAMS UCI).
Mean
Range (2σ)
1624 1540
1578–1670 1468–1612
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Fig. 4. Vertical profiles of bio-elements and Pb in sediments, and δ15N, δ13C and C/N in penguin feathers from PI core. The black dashed lines in δ15N profile indicate the mean value between different periods.
There is no isotope data of present-day Emperor penguin from Amanda Bay to date. Only one study reported the feather isotopic values of Emperor penguin from Terre Adélie Land, East Antarctica, with a mean δ15N values of 12.6 ± 0.5 in 1950s, 13.0 ± 0.3 in 1970s, and 12.1 ± 0.3 in 2000s, respectively (Jaeger and Cherel, 2011). Due to the differences in geography and regional food chains, these N isotope values of extant Emperor penguin at Terre Adélie Land have less meaning in comparative purpose with those of sedimentary penguin feathers from Amanda Bay in this study. δ15N values of emperor penguins mainly depend on the baseline of the food web and penguin dietary compositions. Stable N isotope values of emperor penguin show significant differences between CE 1540– 1866 (Little Ice Age) and CE 1866–2008, indicated an obvious change
in penguin dietary composition or δ15N values of the primary producer (baseline). However, it was reported that the δ15N values of the primary producer in Southern Ocean are higher during cold climate periods and lower during warm periods (Crosta and Shemesh, 2002), opposite to the observed lower δ15N values of penguins during the cold Little Ice Age in our study. Therefore we argue that the temporal variations of δ15N in penguin feathers cannot be attributed to the variation of baseline but primarily to the change of penguin dietary composition. Dietary compositions of emperor penguin vary through geographical sites and seasons (Zimmer et al., 2007). Emperor penguins in Amanda Bay feed mainly on fish, squid and crustaceans, with dominantly silverfish (Pleurogramma antarcticumin) in spring and increasing proportion of crustaceans in early summer (Green, 1986; Gales et al., 1990).
Table 2 Correlation coefficients among the elements in the PI sediments.
TC TN TS TH P Hg Se Cd Cu Zn Pb
TC
TN
TS
TH
P
Hg
Se
Cd
Cu
Zn
Pb
1.00 0.96⁎ 0.49 0.99⁎ 0.81⁎ 0.95⁎ 0.93⁎ 0.94⁎ 0.97⁎ 0.92⁎ −0.86⁎
1.00 0.34 0.95⁎ 0.77⁎ 0.99⁎ 0.94⁎ 0.87⁎ 0.94⁎ 0.92⁎ −0.75⁎
1.00 0.48 0.55 0.38 0.27 0.36 0.36 0.23 −0.64⁎
1.00 0.82⁎ 0.94⁎ 0.92⁎ 0.93⁎ 0.96⁎ 0.93⁎ −0.88⁎
1.00 0.77⁎ 0.80⁎ 0.76⁎ 0.77⁎ 0.82⁎ −0.88⁎
1.00 0.93⁎ 0.88⁎ 0.95⁎ 0.91⁎ −0.74⁎
1.00 0.95⁎ 0.95⁎ 0.98⁎ −0.81⁎
1.00 0.98⁎ 0.95⁎ −0.84⁎
1.00 0.96⁎ −0.81⁎
1.00 −0.81⁎
1.00
⁎ Significant at the 0.01 level (2-tailed).
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δ15N values of emperor penguins reflect their diets and vary through the effects of local climate, topography and/or hydrology on prey availability. The depleted N isotope ratios of penguins during the Little Ice Age may be due to the blocked fish availability by cold climate. For example in the southern Ross Sea, analyses of stomach contents and δ15N in toenails showed that Adélie penguins (Pygoscelis adeliae) consume less silverfish during cold years with increasing sea ice extent (Ainley et al., 1998, 2003). From identification of prey taxa preserved in the ornithogenic soils, Polito et al. (2002) found that silverfish had decreased in the diets of Adélie penguin at Ross Island over the past 600 years, perhaps in response to the onset of the Little Ice Age. Depleted δ15N ratios were recorded in Adélie penguins at Vestfold Hills during the Holocene cold intervals with extensive sea ice, which indicated that penguins consumed less 15N-enriched fish (Huang et al., 2013). In addition to the change of climate or oceanography on prey availability, intra/inter-specific competition may also affect emperor penguin dietary compositions. As it shown in Fig 4, the record of emperor penguin population size inferred from bio-elements varied with their dietary change from N isotopic ratios. High penguin populations occurred with depleted N isotope ratios indicated that emperor penguins consumed less 15N-enriched fish during the Little Ice Age, as the high level populations may cause intensified competition for food resources. For example, many studies have shown that dietary changes within a seabird species were closely linked with their recruitment or population size (Trivelpiece et al., 2011; Wiley et al., 2013). δ13C values of emperor penguins enriched from − 23.88‰ to − 21.82‰ with fluctuations during CE 1540–1891 (Fig 4), suggest a closer to inshore/benthic foraging habitat for emperor penguin populations. Depleting δ13C values of emperor penguin from CE 1891 to 2008 may suggest a progressive variation for penguin foraging niche; this depletion was also likely caused by the shift in δ13C baseline because it was overlapped in time with the accelerating decrease in δ13C in the surface ocean waters since the industrial revolution. The latter is the ‘Suess Effect’, caused by the fact that 13C-depleted CO2 introduced into the atmosphere by the burning of fossil fuels, and the subsequent influx of this 13 C-depleted CO2 into the ocean (Keeling, 1979; Gruber et al., 1999). However, the similar mean δ13C values of emperor penguin between CE 1891–2008 and CE 1540–1891 indicate that the ‘Suess Effect’ in Antarctic Ocean is weaker. 5. Conclusion Based on geochronological, elemental and stable isotope analyses on ornithhogenic sediments and penguin feather remains in PI sediment core, we conclude that emperor penguin colonized at Amanda Bay as early as CE 1540. Emperor penguin population size inferred from bio-elements in PI show high level during the Little Ice Age on N island, opposite to the record of Adélie penguins from the adjacent Vestfold Hills. Depleted N isotope ratios of emperor penguins during the Little Ice Age (CE 1540–1866) were observed, and it could be due to the cold climate related impacts on penguins' prey availability and the potential inter-specific competition. We could provide only a single sediment core from one site at present in this study. In the future, further analyses on modern and sub-fossil samples in other areas in Antarctica should be performed in order to support the results of this study. Conflict of interest The authors declare no conflict of interests. Acknowledgements This work was supported by National Natural Science Foundation of China (Nos. 41476165 and 41106162), Chinese Polar Environment Comprehensive Investigation & Assessment Programmes (CHINA RE2016-02-01, CHINARE2016-04-04), Anhui Provincial Natural Science
Foundation (1308085MD56) and the High-level scientific research foundation for the introduction of talent in Anhui University (J01006033). We thank the Chinese Arctic and Antarctic Administration and Polar Research Institute of China for logistical support and Drs. Tang Jie and Lu Changgui for help in field work.
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Late Holocene Adélie penguin population dynamics at Zolotov Island, Vestfold Hills, Antarctica. J. Paleolimnol. 45, 273–285. Huang, T., Sun, L.G., Stark, J., Wang, Y.H., Cheng, Z.Q., Yang, Q.C., et al., 2011b. Relative changes in krill abundance inferred from Antarctic fur seal. PLoS One 6, e27331. Huang, T., Sun, L.G., Long, N.Y., Wang, Y.H., Huang, W., 2013. Penguin tissue as a proxy for relative krill abundance in East Antarctica during the Holocene. Sci. Rep. 3, 2807. Huang, T., Sun, L.G., Wang, Y.H., Chu, Z.D., Qin, X.Y., Yang, L.J., 2014a. Transport of nutrients and contaminants from ocean to island by emperor penguins from Amanda Bay, East Antarctic. Sci. Total Environ. 468, 578–583. Huang, T., Sun, L.G., Wang, Y.H., Emslie, S.D., 2014b. Paleodietary changes by penguins and seals in association with Antarctic climate and sea ice extent. Chin. Sci. Bull. 59 (33), 4456–4464.
T. Huang et al. / Science of the Total Environment 565 (2016) 1185–1191 Hughen, K.A., Baillie, M.G.L., Bard, E., Beck, J.W., Bertrand, C.J., Blackwell, P.G., 2004. Marine04 marine radiocarbon age calibration, 0–26 cal kyr BP. Radiocarbon 46, 1059–1086. Jaeger, A., Cherel, Y., 2011. Isotopic investigation of contemporary and historic changes in penguin trophic niches and carrying capacity of the Southern Indian Ocean. PLoS One 6 (2), e16484. Jenouvrier, S., Caswell, H., Barbraud, C., Holland, M., Strœve, J., Weimerskirch, H., 2009. Demographic models and IPCC climate projections predict the decline of an emperor penguin population. Proc. Natl. Acad. Sci. U. S. A. 106 (6), 1844–1847. Keeling, C.D., 1979. The Suess effect: 13carbon-14carbon interrelations. Environ. Int. 2, 229–300. Li, Y.S., Cole-Dai, J.H., Zhou, L.Y., 2009. Glaciochemical evidence in an East Antarctica ice core of a recent (CE 1450–1850) neoglacial episode. J. Geophys. Res. 114, D08117. Liu, X.D., Nie, Y.G., Sun, L.G., Emslie, S.D., 2013. Eco-environmental implications of elemental and carbon isotope distributions in ornithogenic sediments from the Ross Sea region, Antarctica. Geochim. Cosmochim. Acta 117, 99–114. Newsome, S.D., Clementz, M.T., Koch, P.L., 2010. Using stable isotope biogeochemistry to study marine mammal ecology. Mar. Mamm. Sci. 26, 509–572. Nie, Y.G., Sun, L.G., Liu, X.D., Emslie, S.D., 2015. From warm to cold: migration of Adélie penguins within Cape Bird, Ross Island. Sci. Rep. 5, 11530. Polito, M., Emslie, S.D., Walker, W., 2002. A 1000-year record of Adélie penguin diets in the southern Ross Sea. Antarct. Sci. 14, 327–332. Robertson, G., 1992. Population-size and breeding success of emperor penguins Aptenodytes forsteri at Auster and Taylor Glacier Colonies, Mawson Coast, Antarctica. Emu 92 (2), 65–71. Stuiver, M., Reimer, P.J., Reimer, R., 2005. CALIB radiocarbon calibration. Execute Version. 5(2). Sun, L.G., Xie, Z.Q., 2001. Relics: penguin population programs. Sci. Prog. 84 (1), 31–44. Sun, L.G., Xie, Z.Q., Zhao, J.L., 2000. A 3,000-year record of penguin populations. Nature 407, 858. Sun, L.G., Emslie, S.D., Huang, T., Blais, J.M., Xie, Z.Q., Liu, X.D., et al., 2013. Vertebrate records in polar sediments: biological responses to past climate change and human activities. Earth-Sci. Rev. 126, 147–155. Trathan, P.N., Fretwell, P.T., Stonehouse, B., 2011. First recorded loss of an emperor penguin colony in the recent period of Antarctic regional warming: implications for other colonies. PLoS One 6 (2), e14738.
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Trivelpiece, W.Z., Hinke, J.T., Miller, A.K., Reiss, C.S., Trivelpiece, S.G., Watters, G.M., 2011. Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proc. Natl. Acad. Sci. U. S. A. 108 (18), 7625–7628. Trull, T.W., Armand, L., 2001. Insights into Southern Ocean carbon export from the δ13C of particles and dissolved inorganic carbon during the SOIREE iron release experiment. Deep Sea Res., Part II 48 (11), 2655–2680. Wienecke, B., 2010. The history of the discovery of emperor penguin colonies, 1902–2004. Polar Rec. 46 (03), 271–276. Wienecke, B., Pedersen, P., 2009. Population estimates of emperor penguins at Amanda Bay, Ingrid Christensen Coast, Antarctica. Polar Rec. 45 (03), 207–214. Wiley, A.E., Ostrom, P.H., Welch, A.J., Fleischer, R.C., Gandhi, H., Southon, J.R., 2013. Millennialscale isotope records from a wide-ranging predator show evidence of recent human impact to oceanic food webs. Proc. Natl. Acad. Sci. U. S. A. 110 (22), 8972–8977. Wilson, E.A., 1907. Aves in British National Antarctic Expedition Report 1901–1904. Nat. Hist. 2, 1–121. Xie, Z., Sun, L., 2008. A 1,800-year record of arsenic concentration in the penguin dropping sediment, Antarctic. Environ. Geol. 55 (5), 1055–1059. Younger, J.L., Clucas, G.V., Kooyman, G., Wienecke, B., Rogers, A.D., Trathan, P.N., et al., 2015. Too much of a good thing: sea ice extent may have forced emperor penguins into refugia during the last glacial maximum. Glob. Chang. Biol. 21 (6), 2215–2226. Younger, J.L., van den Hoff, J., Wienecke, B., Hindell, M., Miller, K.J., 2016a. Contrasting responses to a climate regime change by sympatric, ice-dependent predators. BMC Evol. Biol. 16 (1), 1. Younger, J.L., Emmerson, L.M., Miller, K.J., 2016b. The influence of historical climate changes on Southern Ocean marine predator populations: a comparative analysis. Glob. Chang. Biol. 22 (2), 474–493. Zdanowski, M.K., Zmuda, M.J., Zwolska, W., 2005. Bacterial role in the decomposition of marine-derived material (penguin guano) in the terrestrial maritime Antarctic. Soil Biol. Biochem. 37, 581–595. Zimmer, I., Piatkowski, U., Brey, T., 2007. The trophic link between squid and the emperor penguin Aptenodytes forsteri at Pointe Géologie, Antarctica. Mar. Biol. 152 (5), 1187–1195.
Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Geochemical record of high emperor penguin populations during the Little Ice Age at Amanda Bay, Antarctica Tao Huang a,b,⁎, Lianjiao Yang b, Zhuding Chu b, Liguang Sun b,⁎⁎, Xijie Yin c a b c
School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026, China Third Institute of Oceanography, State Oceanic Administration, Xiamen 361005, China
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Emperor penguin colonized at Amanda Bay, East Antarctic as early as AD 1540. • Populations of emperor penguin at Amanda Bay increase during the little ice age. • Depleted N isotope ratios of Emperor penguins during the LIA were observed.
a r t i c l e
i n f o
Article history: Received 25 March 2016 Received in revised form 19 May 2016 Accepted 23 May 2016 Available online 31 May 2016 Editor: F. Riget Keywords: Emperor penguin Stable isotope analysis Bio-elements Little Ice Age Foraging habitat Sea ice
a b s t r a c t Emperor penguins (Aptenodytes forsteri) are sensitive to the Antarctic climate change because they breed on the fast sea ice. Studies of paleohistory for the emperor penguin are rare, due to the lack of archives on land. In this study, we obtained an emperor penguin ornithogenic sediment profile (PI) and performed geochronological, geochemical and stable isotope analyses on the sediments and feather remains. Two radiocarbon dates of penguin feathers in PI indicate that emperor penguins colonized Amanda Bay as early as CE 1540. By using the bio-elements (P, Se, Hg, Zn and Cd) in sediments and stable isotope values (δ15N and δ13C) in feathers, we inferred relative population size and dietary change of emperor penguins during the period of CE 1540–2008, respectively. An increase in population size with depleted N isotope ratios for emperor penguins on N island at Amanda Bay during the Little Ice Age (CE 1540–1866) was observed, suggesting that cold climate affected the penguin's breeding habitat, prey availability and thus their population and dietary composition. © 2016 Elsevier B.V. All rights reserved.
⁎ Correspondence to: T. Huang, School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China. ⁎⁎ Corresponding author. E-mail addresses: [email protected] (T. Huang), [email protected] (L. Sun).
http://dx.doi.org/10.1016/j.scitotenv.2016.05.166 0048-9697/© 2016 Elsevier B.V. All rights reserved.
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1. Introduction The emperor penguin (Aptenodytes forsteri) is known to be extremely sensitive to changes in climate and sea ice dynamics. Recent model studies have estimated that at least two-thirds of emperor penguin colonies will have dramatically declined by more than half at the end of this century if sea ice extent decrease at the rate predicted by the Intergovernmental Panel on Climate Change (IPCC) (Jenouvrier et al., 2009; Ainley et al., 2010). Since it breeds on the fast sea ice and feeds only at sea, its population size and foraging behavior are affected dominantly by marine environmental variability. For example, census data from Terre Adélie show that the emperor penguins have declined by N50% during the late 1970s when there was an abnormally warm period with reduced sea-ice extent (Barbraud and Weimerskirch, 2001). Since 1902 when the first breeding colony was discovered (Wilson, 1907), many studies using the methods of ground counts, aerial photos and remote sensing have provided more and more information on the populations, colonies and foraging habitat of emperor penguin around the Antarctic continent (e.g. Robertson, 1992; Cherel and Kooyman, 1998; Barber-Meyer et al., 2007; Wienecke and Pedersen, 2009; Fretwell and Trathan, 2009; Wienecke, 2010; Trathan et al., 2011; Fretwell et al., 2012, 2014). Unlike Pygoscelis penguins which have left an extensive records of their occupation history, population size and dietary change in the ornithogenic soils and sediments (e.g. Sun et al., 2000, 2013; Emslie and Patterson, 2007, Emslie et al., 2014), the emperor penguins have been less studied for their paleohistory due to the lack of archives on land because most of their remains are lost to the ocean when the sea ice melts in summer. Using mitochondrial DNA from modern colonies and sub-fossil remains, Younger et al. present that emperor penguin population expanded several-fold during the Holocene from the Last Glacial Maximum (LGM), which suggests an optimal sea ice condition occur for this species, corresponding to accessible foraging habitat (Younger et al., 2015, 2016a, 2016b). These genetic studies investigated how emperor penguin populations were affected by climate changes during and following the LGM, though the resolution is relative low over shorter timescales. During field investigations, we observed
many emperor penguins on an island around Amanda Bay, East Antarctic. Those emperor penguins have transferred a large amount of nutrients and contaminants from ocean to land and formed penguin ornithogenic sediments (Huang et al., 2014a). In this study we collect a penguin ornithogenic sediment core (PI) at Amanda Bay, establish its chronology by radiometric and radiocarbon dating, and reconstruct the population size and dietary changes of visited emperor penguins by geochemical markers (bio-elements and stable isotopes) in PI sediments and organic remains.
2. Materials and methods 2.1. Sample collection and chronology The penguin ornithogenic sediment core was collected at the N island, on the southwest side of the Amanda Bay, Ingrid Christensen Coast of Princess Elizabeth Land, East Antarctica (Fig. 1) in 2008. During the field season, a 9-cm diameter PVC pipe was pushed vertically into the centre of the pond to collect a core and named it as PI. In the laboratory, this 14-cm-long core was sectioned at 0.5 cm intervals on the top 4.5 cm and 1.0 cm below 4.5 cm, to obtain a total of 20 subsamples. Penguin remains such as feathers and bones were picked from each subsample. Before chemical analyses, each subsample was air-dried in a clean laboratory and homogenized. To establish the chronology of PI, we performed radiometric dating (210Pb, 137Cs) and AMS14C dating. 210Pb, 226Ra and 137Cs dating was performed on each subsample by direct gamma spectrometry using an Ortec HPGe GWL series detector. In addition, two feather samples from the bottom of PI (13 and 14 cm depths) were dated by AMS14C analysis at W.M. Keck Carbon Cycle Accelerator Mass Spectrometry Laboratory, University of California Irvine. The conventional radiocarbon dates were corrected and calibrated using the CALIB 5.1.0 program (Stuiver et al., 2005) and the dataset of Marine04 (Hughen et al., 2004), with a marine reservoir effect (ΔR) of 1700 years. This ΔR was selected based on the fact that modern marine algae have a 14C age of 1700 years in East Antarctic ocean (Domack et al., 1991).
Fig. 1. Study area and the sampling site PI near Amanda Bay, East Antarctic.
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2.2. Elemental and stable isotope analyses The concentrations of element P, Cu, Zn, Pb, Hg and Se, stable carbon and nitrogen isotope values as well as the ratios of C/N in the sediments of PI were analyzed and published in Huang et al. (2014a). In this study, the concentration of Cd in PI sediments was analyzed by using the same method in Huang et al. (2014a). Contents of Total Carbon (TC), Total Nitrogen (TN), Total Sulfur (TS) and Total Hydrogen (TH) were measured by vario EL III (Elementar, Germany) with a relative error of 0.1%. Twenty feather samples picked from each subsample of PI were analyzed for the stable C and N isotopes as well as C/N ratios. Samples were cleaned with Millipore water and 2:1 chloroform: methanol solution, and then dried at 40 °C. Samples and standards were weighed accurately into tin capsules and loaded into element analyzer-isotope ratio mass spectrometer (Flash EA1112 HT- 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 deviation of the insert standard samples (n = 5) is b0.25‰ for δ13C, b 0.20‰ for δ15N, and b0.2% and b0.2% for C and N content, respectively. Stable isotope results are presented in δ (‰) and expressed relative to air for δ15N and Vienna Pee Dee Belemnite (VPDB) for δ13C according to the equation: δ (‰) = [(Rsample − Rstandard)/Rstandard] ∗ 103, where δ (‰) represents the δ15N or δ13C value, Rsample is the isotopic ratio of the sample, and Rstandard the isotopic ratio of the air and VPDB. 2.3. Statistical test for isotopic and elemental data in PI
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sediments of PI are 15.5 ± 1.6% (mean ± standard error of mean, 5.4%–30.7%, n = 20), 2.7 ± 0.3% (0.8–6.0%, n = 20), 0.6 ± 0.1% (0.2%– 1.2%, n = 20) and 2.0 ± 0.3% (0.2%–4.4%, n = 20), respectively. TC, TN and TH show similar decreasing trend from bottom to top in the profile. The data of TC/TN, δ15N and δ13C in sediments suggested a source of penguin-derived organic materials for PI (Huang et al., 2014a). Geochronological results for PI are shown in Fig. 3 and Table 1. The activity of 210Pb in PI displayed a down trend with fluctuations against depth, while that of 226Ra was increasing in the top 2 cm and then decreasing gradually (Fig. 3a). They came to equilibration at 9.0 cm, indicating the decreasing excess 210Pb reached its zero point. A CRS (Constant Rate of Supply) model was used for 210Pb dating calculation (Appleby, 2001) and PI was dated back to CE 1827 at the depth of 9.0 cm. The signal of 137Cs in PI was weak and showed a decreasing trend with two peaks at the surface and the depth of 2.0 cm, respectively. The later might be corresponding to the Chernobyl nuclear accident in 1986. However, there is no signature for the bomb testing in 1960s. In addition, two radiocarbon results are shown in Table 1. The mean calibrated ages of penguin feathers at 13 and 14 cm are about CE 1624 and 1540, respectively. The chronology of PI was established using polynomial interpolation by these two 14C dates and the 210Pb dates in the top 9.0 cm which were fitted well in the regression line (Fig. 3b). 3.2. Elemental concentrations in PI sediments
We ran Pearson correlation analysis on concentrations of elements and TC, TN, TS, TH using SPSS16.0, to examine the relationship between elements and TC, TN, TS, TH in the sediments. To assess the significance of the difference in stable isotope ratios between different periods, we performed two-step statistical tests in 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 the stable isotope data in PI follow normal distribution. Second, we performed parametric independent samples t-test and used 0.05 for the level of significance.
The concentration data of phosphorus (P), selenium (Se), mercury (Hg), copper (Cu), zinc (Zn) and lead (Pb) in PI sediments were published in Huang et al. (2014a). The mean concentration of cadmium (Cd) in sediments of PI is 3.0 ± 0.3 mg kg−1 (1.0–5.7 mg kg− 1, n = 20). Overall, the elements P, Se, Hg, Cu, Zn and Cd show a very similar decreasing trend from bottom to top in their profile, with a higher level at the depth of 8.5–14 cm and low between 8.0 and 0 cm (Fig. 4). Element of Pb, however, shows an opposite vertical trend in comparison with those of other 6 elements. Pearson correlation analyses on these elements and TC, TN, TS and TH were performed and the results are listed in Table 2. P, Se, Hg, Cu, Zn, Cd, TC, TN and TH are significantly correlated with each other and they are negatively correlated with Pb.
3. Results
3.3. Stable isotope values in penguin feathers
3.1. Sedimentology and chronology
The C/N ratios of the penguin feathers in PI range from 3.03% to 3.39% with a mean of 3.17 ± 0.02% (n = 20); they remain stable in the studied time period (Fig 4), indicating a good preservation of the penguin feathers. The δ13C values in the penguin feathers range from − 21.32‰ to − 23.88‰ with a mean of − 22.86 ± 0.16‰ (n = 20); the δ15N values have a greater range from 11.68‰ to 19.18‰ with a mean of 14.85 ± 0.42‰ (n = 20). For the overall profile, the δ15N values show an increasing trend over time, while δ13C values do not. Depleted
PI is a 14-cm-long core with a homogeneous sedimentary characteristic (Fig. 2). It consists of olive to dark olive clay with many physical penguin remains such as bones and feathers, and has a strong smell of penguin guano. PI was identified as an ornithogenic sediment profile by the sedimentary characteristic and geochemical compositions in sediments (Huang et al., 2014a). The total contents of C, N, S and H in
Fig. 2. The sedimentology and concentration profiles of TC, TN, S, TH, δ15N, δ13C and TC/TN in PI sediments.
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Fig. 3. Geochronological results of PI. a: Activity of radionuclides measured in the PI sediments. b: the age profile of PI based on the 210Pb and 14C dates.
penguin N isotope ratios (13.45 ± 0.55, n = 7) occurred from CE 1540 to 1866 during the Little Ice Age (LIA), while high N isotope values (15.60 ± 0.46, n = 13) of penguins between CE 1866–2008. Emperor penguins show a significant difference (t = 2.879, p = 0.01) in their N isotope values between CE 1540–1866 and 1866–2008. 4. Discussion
here to track activities of emperor penguin populations. Therefore, concentrations of these bio-elements in PI are considered to be geochemical markers for changes in emperor penguin guano inputs and thus penguin population size around the pond catchment. Specifically, high concentration of bio-elements indicates high level guano inputs and thus greater penguin numbers. The level of bio-elements in PI indicates high emperor penguin population size during the year of CE 1540–1866, and low between CE 1891–2008 in N island, Amanda Bay (Fig. 4). It should be noted that the inferred high emperor penguin population size during CE 1540– 1866 corresponds to a recent neoglacial episode or Little Ice Age (CE 1450–1850) as recorded in an ice core from the Princess Elizabeth Land, East Antarctica (Li et al., 2009). Such association may be explained by the impacts of climate-related changes on this sea-ice breeding species. During the period of neoglacial climates, extended sea ice cover provides ample nesting and breeding sites for emperor penguins. This change is opposite to that of Adélie penguins on Vestfold Hills which decreased in population size during the Little Ice Age (Huang et al., 2011a), as more snow or ice cover on land during cold climate making it harder for the land breeding Adélie penguins to nest and breed. It should be noted that the effective emperor population sizes are smaller during the LGM which is likely due to the severely restricted foraging habitat available for penguins (Younger et al., 2015, 2016a). In this study, the geochemical evidence of high penguin populations during the LIA implies an unrestricted access to foraging area for emperor penguins at that time period. This is likely because the climate during the LIA in Antarctica is mild in contrast to that in northern hemisphere (Bertler et al., 2011). Indeed, it has been proposed that there is an optimal sea ice condition at the large spatio-temporal scale for emperor penguins, corresponding to ample breeding sites and available foraging area (Ainley et al., 2010; Younger et al., 2015). The inferred emperor penguin populations declined from CE 1978 (Fig. 4), similar to that decrease in the observational emperor penguin populations in Terre Adélie Land, East Antarctica during the late 1970s when there was an abnormally warm period with reduced sea-ice extent (Barbraud and Weimerskirch, 2001).
4.1. Bio-elements as geochemical markers for emperor penguin populations 4.2. Dietary change of emperor penguins from feather isotopic signature Many elements are enriched in seabird guanos, ornithogenic soils and sediments, and they are considered as bio-elements and indicators of sources from seabird activities (Sun and Xie, 2001, Sun et al., 2013; Blais et al., 2007; Emslie et al., 2014). In Antarctica for Pygoscelis penguin species, these reported bio-elements include F, P, S, Se, Cu, Zn, Ca, Sr, Be, As, Fe, Mg and Mn in Ardley Island and King George Island, South Shetland Islands (Sun et al., 2000; Zdanowski et al., 2005; Xie and Sun, 2008), F, P, S, Se, Cu, Sr, Cd, Mg and As in Vestfold hills (Huang et al., 2009, 2011a), and F, P, S, Mg, Ca, Hg, Se, As, Cu, Zn, and Cd in Ross Island and Victoria Land along the Ross Sea (Hofstee et al., 2006; Liu et al., 2013; Nie et al., 2015). Our geochemical analyses on PI sediments and local mother rock indicated that elements P, Hg, Se, Zn and Cd are enriched in emperor penguin ornithogenic sediments, with the high Igeo values (geoaccumulation indexes) of 2.8, 2.9, 5.6 and 1.2 for P, Hg, Se and Zn, respectively (Huang et al., 2014a). The Igeo of Cd was not calculated since its very low level in mother rock which is below the detection limit of the analytical techniques. These marine-derived elements are transported to terrestrial environment by penguins in the form of guanos and/or dead bodies, and thus they are defined as bio-elements
Stable carbon and nitrogen isotope ratios in tissues have been used extensively in tracing marine animal foraging habitats, trophic level or diets and migration patterns (Cherel and Hobson, 2007; Newsome et al., 2010; Huang et al., 2011b, 2014b). This is based on the fact that in marine environments, the stable nitrogen isotope ratio (15N/14N, δ15N) shows an enrichment of ~ 3‰–5‰ from prey to consumer, and it could therefore be used as an indicator for the diet and trophic level of marine predators (Hobson et al., 1994). In contrast, the carbon isotope ratio (13C/12C, δ13C) vary little through the marine food chain (b 1‰) but changes remarkably between habitats. For example, δ13C signature of particulate organic matter increases from offshore to inshore waters (Trull and Armand, 2001), and δ13C could serves as a carbon source tracer and provide information on the foraging habitat of the studied consumers (Cherel et al., 2011). Stable isotopes in tissues have different turnover rates and time scales, from days for blood, to weeks for feathers (Bearhop et al., 2003). Carbon and nitrogen isotopic signatures in penguin feathers reflect those of the average diets at the time of feather growth.
Table 1 14 C dates and calibrated ages using CALIB 5.1.0 and the Marine04 datasets (ΔR: 1700 ± 30). Calibrated age (CE) UCIAMS number
Sample number
Sample material
Depth (cm)
Conventional
55720 55719
PI-19 PI-20
Feather Feather
13 14
2410 ± 15 2445 ± 15
14
C age (yr BP)
Note: The dates are measured at the W.M. Keck Carbon Cycle Accelerator Mass Spectrometry Laboratory, University of California Irvine (KCCAMS UCI).
Mean
Range (2σ)
1624 1540
1578–1670 1468–1612
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Fig. 4. Vertical profiles of bio-elements and Pb in sediments, and δ15N, δ13C and C/N in penguin feathers from PI core. The black dashed lines in δ15N profile indicate the mean value between different periods.
There is no isotope data of present-day Emperor penguin from Amanda Bay to date. Only one study reported the feather isotopic values of Emperor penguin from Terre Adélie Land, East Antarctica, with a mean δ15N values of 12.6 ± 0.5 in 1950s, 13.0 ± 0.3 in 1970s, and 12.1 ± 0.3 in 2000s, respectively (Jaeger and Cherel, 2011). Due to the differences in geography and regional food chains, these N isotope values of extant Emperor penguin at Terre Adélie Land have less meaning in comparative purpose with those of sedimentary penguin feathers from Amanda Bay in this study. δ15N values of emperor penguins mainly depend on the baseline of the food web and penguin dietary compositions. Stable N isotope values of emperor penguin show significant differences between CE 1540– 1866 (Little Ice Age) and CE 1866–2008, indicated an obvious change
in penguin dietary composition or δ15N values of the primary producer (baseline). However, it was reported that the δ15N values of the primary producer in Southern Ocean are higher during cold climate periods and lower during warm periods (Crosta and Shemesh, 2002), opposite to the observed lower δ15N values of penguins during the cold Little Ice Age in our study. Therefore we argue that the temporal variations of δ15N in penguin feathers cannot be attributed to the variation of baseline but primarily to the change of penguin dietary composition. Dietary compositions of emperor penguin vary through geographical sites and seasons (Zimmer et al., 2007). Emperor penguins in Amanda Bay feed mainly on fish, squid and crustaceans, with dominantly silverfish (Pleurogramma antarcticumin) in spring and increasing proportion of crustaceans in early summer (Green, 1986; Gales et al., 1990).
Table 2 Correlation coefficients among the elements in the PI sediments.
TC TN TS TH P Hg Se Cd Cu Zn Pb
TC
TN
TS
TH
P
Hg
Se
Cd
Cu
Zn
Pb
1.00 0.96⁎ 0.49 0.99⁎ 0.81⁎ 0.95⁎ 0.93⁎ 0.94⁎ 0.97⁎ 0.92⁎ −0.86⁎
1.00 0.34 0.95⁎ 0.77⁎ 0.99⁎ 0.94⁎ 0.87⁎ 0.94⁎ 0.92⁎ −0.75⁎
1.00 0.48 0.55 0.38 0.27 0.36 0.36 0.23 −0.64⁎
1.00 0.82⁎ 0.94⁎ 0.92⁎ 0.93⁎ 0.96⁎ 0.93⁎ −0.88⁎
1.00 0.77⁎ 0.80⁎ 0.76⁎ 0.77⁎ 0.82⁎ −0.88⁎
1.00 0.93⁎ 0.88⁎ 0.95⁎ 0.91⁎ −0.74⁎
1.00 0.95⁎ 0.95⁎ 0.98⁎ −0.81⁎
1.00 0.98⁎ 0.95⁎ −0.84⁎
1.00 0.96⁎ −0.81⁎
1.00 −0.81⁎
1.00
⁎ Significant at the 0.01 level (2-tailed).
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δ15N values of emperor penguins reflect their diets and vary through the effects of local climate, topography and/or hydrology on prey availability. The depleted N isotope ratios of penguins during the Little Ice Age may be due to the blocked fish availability by cold climate. For example in the southern Ross Sea, analyses of stomach contents and δ15N in toenails showed that Adélie penguins (Pygoscelis adeliae) consume less silverfish during cold years with increasing sea ice extent (Ainley et al., 1998, 2003). From identification of prey taxa preserved in the ornithogenic soils, Polito et al. (2002) found that silverfish had decreased in the diets of Adélie penguin at Ross Island over the past 600 years, perhaps in response to the onset of the Little Ice Age. Depleted δ15N ratios were recorded in Adélie penguins at Vestfold Hills during the Holocene cold intervals with extensive sea ice, which indicated that penguins consumed less 15N-enriched fish (Huang et al., 2013). In addition to the change of climate or oceanography on prey availability, intra/inter-specific competition may also affect emperor penguin dietary compositions. As it shown in Fig 4, the record of emperor penguin population size inferred from bio-elements varied with their dietary change from N isotopic ratios. High penguin populations occurred with depleted N isotope ratios indicated that emperor penguins consumed less 15N-enriched fish during the Little Ice Age, as the high level populations may cause intensified competition for food resources. For example, many studies have shown that dietary changes within a seabird species were closely linked with their recruitment or population size (Trivelpiece et al., 2011; Wiley et al., 2013). δ13C values of emperor penguins enriched from − 23.88‰ to − 21.82‰ with fluctuations during CE 1540–1891 (Fig 4), suggest a closer to inshore/benthic foraging habitat for emperor penguin populations. Depleting δ13C values of emperor penguin from CE 1891 to 2008 may suggest a progressive variation for penguin foraging niche; this depletion was also likely caused by the shift in δ13C baseline because it was overlapped in time with the accelerating decrease in δ13C in the surface ocean waters since the industrial revolution. The latter is the ‘Suess Effect’, caused by the fact that 13C-depleted CO2 introduced into the atmosphere by the burning of fossil fuels, and the subsequent influx of this 13 C-depleted CO2 into the ocean (Keeling, 1979; Gruber et al., 1999). However, the similar mean δ13C values of emperor penguin between CE 1891–2008 and CE 1540–1891 indicate that the ‘Suess Effect’ in Antarctic Ocean is weaker. 5. Conclusion Based on geochronological, elemental and stable isotope analyses on ornithhogenic sediments and penguin feather remains in PI sediment core, we conclude that emperor penguin colonized at Amanda Bay as early as CE 1540. Emperor penguin population size inferred from bio-elements in PI show high level during the Little Ice Age on N island, opposite to the record of Adélie penguins from the adjacent Vestfold Hills. Depleted N isotope ratios of emperor penguins during the Little Ice Age (CE 1540–1866) were observed, and it could be due to the cold climate related impacts on penguins' prey availability and the potential inter-specific competition. We could provide only a single sediment core from one site at present in this study. In the future, further analyses on modern and sub-fossil samples in other areas in Antarctica should be performed in order to support the results of this study. Conflict of interest The authors declare no conflict of interests. Acknowledgements This work was supported by National Natural Science Foundation of China (Nos. 41476165 and 41106162), Chinese Polar Environment Comprehensive Investigation & Assessment Programmes (CHINA RE2016-02-01, CHINARE2016-04-04), Anhui Provincial Natural Science
Foundation (1308085MD56) and the High-level scientific research foundation for the introduction of talent in Anhui University (J01006033). We thank the Chinese Arctic and Antarctic Administration and Polar Research Institute of China for logistical support and Drs. Tang Jie and Lu Changgui for help in field work.
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