Science of the Total Environment 468–469 (2014) 578–583
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Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv
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
H I G H L I G H T S
• 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
a r t i c l e
i n f o
Article history:
Received 13 June 2013
Received in revised form 26 August 2013
Accepted 26 August 2013
Available online xxxx
Editor: Frank Riget
Keywords:
Emperor penguin
Ornithogenic sediments
Bio-transfer
Stable isotope analysis
Nutrients and contaminants
a b s t r a c t
Penguins play important roles in the biogeochemical cycle between Antarctic Ocean and land ecosystems. The
roles of emperor penguin Aptenodytes forsteri, however, are usually ignored because emperor penguin breeds
in fast sea ice. In this study, we collected two sediment profiles (EPI and PI) from the N island near a large emperor penguin colony at Amanda Bay, East Antarctic and performed stable isotope and element analyses. The organic
C/N ratios and carbon and nitrogen isotopes suggested an autochthonous source of organic materials for the sediments of EPI (C/N = 10.21 ± 0.28, n = 17; δ13C = −13.48 ± 0.50‰, δ15N = 8.35 ± 0.55‰, n = 4) and an
allochthonous source of marine-derived organic materials for the sediments of PI (C/N = 6.15 ± 0.08,
δ13C = −26.85 ± 0.11‰, δ15N = 21.21 ± 2.02‰, n = 20). The concentrations of total phosphorus (TP), selenium (Se), mercury (Hg) and zinc (Zn) in PI sediments were much higher than those in EPI, the concentration of
copper (Cu) in PI was a little lower, and the concentration of element lead (Pb) showed no difference. As measured by the geoaccumulation indexes, Zn, TP, Hg and Se were from moderately to very strongly enriched in
PI, relative to local mother rock, due to the guano input from juvenile emperor penguins. Because of its high trophic 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
As a typical seabird in the Southern Ocean ecosystem, penguins
are good indicator of Antarctic climate change and marine environment status (Ainley, 2002; Boersma, 2008). Plentiful ecological information could be extracted from penguin guanos and ornithogenic
sediments to study those polar vertebrates' population records and
their responses to past climate changes and human activities (Sun
et al., 2013). For example, elemental analyses on lake sediments from
Ardley Island, Vestfold Hills and Ross Island identified elements such
as Sr, F, S, Se, P, Cu and Zn as geochemical markers of penguin guano inputs (Sun et al., 2000; Huang et al., 2009a; Liu et al., 2013). 87Sr/86Sr ratios of marine-derived materials and levels of biomarker fecal sterols in
those lake sediments were determined and identified as good proxy for
⁎ Corresponding author.
E-mail address: [email protected] (L. Sun).
0048-9697/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.scitotenv.2013.08.082
penguin population (Sun et al., 2005; Wang et al., 2007). Radiocarbon
dates of the ornithogenic soils/sediments and tissue remains unveiled
penguin occupation history and their relationship with regional marine
environmental changes and land ice advance and retreat (e.g. Baroni
and Orombelli, 1994; Emslie et al., 2003; Huang et al., 2009b).
Seabirds transport materials from ocean to lake or pond systems in
island and coastal land by guanos, and impact the lake productivities,
the chemical compositions of lake water and sediments, and the structure and diversity of lake biota (e.g. Sánchez-Piñero and Polis, 2000;
Blais et al., 2005, 2007; Ellis et al., 2006; Michelutti et al., 2009, 2011).
Chemical compositions of penguin's guano reflect the status of regional
marine food web chemistry (Roosens et al., 2007). Antarctic land-based
penguins (Adélie, Chinstrap and Gentoo) play important roles in
connecting ocean and land ecosystems, and they transport marinederived nutrients and contaminants to ice free land areas in the form
of guanos or dead bodies (Tatur and Mayrcha, 1984; Sun and Xie,
2001; Huang et al., 2011a). At Ross Island, Ardley Island and Vestfold
T. Huang et al. / Science of the Total Environment 468–469 (2014) 578–583
Hills in Antarctica, Pygoscelis penguins could transfer about 4.0 × 105 kg
of phosphorus per year from ocean to islands and coastal lands (Qin
et al., 2013). Pygoscelis penguins transported large amounts of marine
heavy metals and organic pollutants from both natural and anthropogenic sources to lands, lakes or ponds in the form of guanos, feathers
and eggshells (Roosens et al., 2007; Xie and Sun, 2008; Brasso et al.,
2012). These transported nutrients and contaminants were deposited
in land and lakes and then formed penguin ornithogenic soils and sediments. Unlike Pygoscelis penguins, emperor penguins have been less
studied for their roles in the biogeochemical cycle between ocean and
land, likely due to the fact that adult emperor penguins breed in sea
ice and rarely visit land (Le Maho, 1977).
During several field investigations, we observed many juvenile
emperor penguins in the N island near their colony, even though
their population is smaller than that of the land-based Pygoscelis
penguins. To study possible impacts by juvenile emperor penguins
on land environment, in this study, we collected two sediment
cores (named as EPI and PI) from the N island near a large emperor
penguin colony at Amanda Bay, East Antarctic and performed stable
C and N isotope and elemental analyses. By comparing stable isotope
values, elemental concentrations and sedimentary characteristic, we
identified the sources of organic matters in EPI and PI, calculated the
geoaccumulation index of elements in PI, and discussed emperor
penguins' roles in transfer of nutrients and contaminants from
ocean to island and freshwater systems.
2. Materials and methods
2.1. Study area and sample collection
Amanda Bay is located at the Ingrid Christensen Coast of Princess
Elizabeth Land, East Antarctica, about 20 km northeast of Chinese
Zhongshan Station (Larsemann Hills) and nearly 80 km to the west of
Australian Davis Station (Vestfold Hills). It is approximately 3 km
wide and 6 km long, and opens northwest into the much larger Prydz
Bay. The southwest side of the bay is flanked by the Flatnes Ice Tongue.
The eastern and southern sides are bounded by the ice cliffs of the
Hovde Glacier, with Hovde Island in the northeast. There are some
small islands within the bay. Fast ice within the Prydz Bay renders the
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sea ice unstable for most of the year and provides the emperor penguin
colony in Amanda Bay with good access to the sea for feeding. Colonies
of several thousand pairs of emperor penguins occupy variable positions
in the southwest corner of Amanda Bay (Wienecke and Pedersen,
2009).
During the field investigation, two sediment cores (EPI and PI) were
collected at the N island, on the southwest side of the Amanda Bay
(Fig. 1). EPI core was extracted from a pond with a 19 m height above
sea level while PI core was collected from a pond with a 1.5 m height
above sea level. The PI core pond was near the emperor penguin colony
and many penguin feathers and even a little mummified penguin were
found near the pond. In the laboratory, the cores were opened. EPI was
sectioned at 1 cm intervals to obtain 17 subsamples; PI was sectioned at
0.5 cm interval on the top 4.5 cm and at 1.0 cm interval on the layer
below 4.5 cm, to obtain a total of 20 subsamples. Penguin remains
such as bones and feathers were found in PI sediment core and were
handpicked. All the subsamples as well as local bedrock samples were
stored frozen prior to analysis.
2.2. Stable isotope and elemental analysis
All the samples from EPI and PI were analyzed for the organic C/N
ratio; 4 samples in EPI and 20 samples in PI were analyzed for the stable
C and N isotope ratios. Samples were air-dried, powdered, acidified with
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
standards were weighed accurately into tin capsules and loaded into element analyzer–isotope ratio mass spectrometer (Flash EA 1112 HTDelta 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 b0.20‰ for δ13C, b 0.30‰
for δ15N, and b 0.8% and b0.7% 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.
For elemental analyses, about 0.25 g of sediment and bedrock powder was taken, weighed, and digested (HNO3–HF–HClO4) in a Teflon
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.
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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 spectroscopy (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
(δ13C and δ15N, 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 = 17 for
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). Second, we performed parametric independent samples t-test and used
0.05 for the level of significance.
3. Results
3.1. C/N ratios and stable isotopes
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
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). The δ13C
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
range from 15.05‰ to 47.09‰ with a mean of 21.21 ± 2.02‰
(n = 20). The δ13C values in the EPI sediments range from −12.05‰
to −14.29‰ with a mean of −13.48 ± 0.50‰ (n = 4); the δ15N values
range from 6.98‰ to 9.64‰ with a mean of 8.35 ± 0.55‰ (n = 4). Stable C and N isotope values between PI and EPI show a significant difference (δ13C: t = 26.202, p b 0.001; δ15N: t = 6.139, p b 0.001), and
they are plotted vs. C/N ratios in the Fig. 2.
3.2. Elemental concentrations and geoaccumulation index (Igeo)
The mean concentrations of TP, Hg, Se, Zn, Cu and Pb in sediments of PI are 2.5 ± 0.3%, 281 ± 25 ng g − 1, 9.1 ± 1.1 mg kg− 1,
652 ± 86 mg kg−1, 22.3 ± 2.1 mg kg−1 and 23.8 ± 1.7 mg kg−1,
respectively. The mean levels of corresponding elements in EPI
are 0.29 ± 0.01%, 55.5 ± 2.1 ng g− 1, 2.9 ± 0.2 mg kg− 1, 138 ±
19 mg kg− 1, 35.3 ± 3.1 mg kg− 1 and 20.5 ± 1.3 mg kg− 1, respectively. Elemental concentrations vs. C/N ratios in PI and EPI are plotted
in Fig. 3. PI has higher levels of TP, Hg, Se and Zn and lower levels of
Cu than EPI, and the differences are significant for TP, Hg, Se, Zn and
Cu (TP: t = 6.411, p b 0.001; Hg: t = 8.231, p b 0.001; Se: t = 4.979,
p b 0.001, Zn: t = 5.377, p b 0.001, Cu: t = 3.485, p = 0.002) and
insignificant for Pb (t = 1.464, p = 0.152).
The geoaccumulation indexes (Igeo) of 6 elements in PI are shown in
Fig. 4. TP, Hg, Se and Zn have high Igeo values with a mean of 2.8 ± 0.2,
2.9 ± 0.1, 5.6 ± 0.2 and 1.2 ± 0.2, respectively; Cu and Pb have negative Igeo values.
Fig. 2. Isotope values vs. C/N ratios in EPI and PI. a: δ13C, b: δ15N, triangle for PI, and dot for
EPI.
4. Discussion
4.1. Sources of organic matter in PI and EPI
The ecosystem of Antarctic islands and coastal ice free land areas is
relatively simple. The organic matters in Antarctic lake or pond sediments are mainly from autochthonous algae or allochthonous floras
and faunas (e.g. Sun et al., 2013). During the core section, visual inspection showed a homogenous lithostratigraphy for EPI and PI cores. EPI is
composed of mainly peat and PI of mainly black mud with a strong unpleasant smell of penguin guano. Mean C/N ratios of PI and EPI (6.15 ±
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
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
between PI and EPI sediments is significant, we cannot distinguish
their exact original sources since the C/N ratios in PI and EPI are within
the range of both lacustrine and marine organic materials.
δ13C is a useful proxy in tracing organic sources in sediments (Meyers,
1994). The δ13C values of lake algae are usually around −27‰ (Meyers,
1994), but they can increase to reach as high as −9‰ when the algae
begin to use dissolved bicarbonate as the carbon source (Meyers, 2003).
Marine phytoplankton typically has δ13C values between −22‰ and
−20‰, and the δ13C values of particulate organic carbon in Southern
Ocean are around −26‰ (Berg et al., 2011). The mean δ13C value of
−13.48 ± 0.50‰ in the EPI sediments indicates freshwater algae
sedimentation, and this is further supported by the observed sedimentary characteristic. High δ13C values in lake sediments are also
observed in the nearby Larsemann Hills (mean: − 9.90‰, range:
− 11.31‰ – − 8.92‰, n = 63, Liu et al., unpublished results).
These high δ13C values of lake sediments in East Antarctica suggest
T. Huang et al. / Science of the Total Environment 468–469 (2014) 578–583
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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 δ13C values
of the PI sediments range from − 25.76‰ to − 27.35‰ with a
mean of −26.85 ± 0.11‰, indicating either freshwater or marine
Fig. 4. Geoaccumulation index of elements in the PI sediments (data was presented by
mean ± standard error of mean, n = 20).
original organic sources. Since the freshwater algae sedimentations in
both the N island (EPI) and the nearby Larsemann Hills have high δ13C
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 ammonia and heavier nitrogen-15 is enriched in the remaining sediments.
Similarly high nitrogen isotopic ratios are observed in Adélie penguin
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ornithogenic soils (32.2‰, n = 6, Mizutani et al., 1986), Adélie penguin
guanos (25.0‰, n = 3), ornithogenic sediments (28.4‰, n = 11, Huang
et al. unpublished results), and seal excrement sediments (24.0‰, n =
32, Liu et al., 2004). By comparing stable C and N isotope values of PI
and EPI, we conclude that PI sediments are affected by emperor
penguin's guano input while EPI sediments are from natural lake
algae sedimentation.
4.2. Emperor penguins transfer nutrients and contaminants from ocean to
island
The transport of large amount of nutrients and contaminants from
ocean to the Antarctic islands and coastal ice free land areas by the
land-based Pygoscelis penguins have been studied (e.g. Sun and Xie,
2001; Roosens et al., 2007; Nędzarek, 2010). Emperor penguins' role
in such transport, however, is usually ignored because they are sea ice
breeding species (Le Maho, 1977). Our stable isotope analyses suggest
natural lacustrine algae sedimentation in EPI and marine-derived emperor penguin guano deposition in PI. The concentrations of TP, Hg, Se,
and Zn in ornithogenic sediments of PI are much higher than those of
EPI, the concentration of Cu is a little lower, and Pb shows no difference.
Thus, Cu and Pb mainly originate from local mother rock and are not affected by penguin guano input.
The geoaccumulation index (Igeo) by Müller (1979) has been extensively used for evaluating contamination and enrichment of elements in
sediments. Förstner et al. (1993) classified sediments into seven classes
based upon Igeo, from practically unpolluted level (class 0, Igeo b 0) to
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 Igeo value of
5.6 ± 0.8, indicating a very strong enrichment, apparently because of
the very high concentration of Se in emperor penguin ornithogenic sediments and the very low level in local mother rock. High concentration
of Se in Pygoscelis penguin guanos and ornithogenic sediments from
Ardley Island, Victoria Land and Vestfold Hills in Antarctica was also observed (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 ±
0.2 and 2.9 ± 0.1, indicating moderate to strong enrichment and pollution of them, apparently due to penguin guano input. The Igeo of heavy
metal of Zn in PI is 1.2 ± 0.2, a moderately pollution level. The Igeo of
Cu and Pb in PI are negative, indicating that Cu and Pb are not affected
by penguin guano input. Different homeostatic processes from nonessential elements Hg and Pb in contrast to essential elements TP, Se,
Cu and Zn may cause a bias in our dataset. However, the non-essential
element Hg has an Igeo value comparable to that of the essential element
TP and Pb has much lower value of Igeo than TP and Hg; thus the effects
of the homeostatic processes of elements on the dataset in the present
study are likely insignificant. The geoaccumulation index values of elements in PI and EPI showed that juvenile emperor penguins transferred
a large number of nutrients and contaminants from ocean to island
system.
Trophic position of seabirds influences their efficacy in transferring pollutants from ocean to land. Seabirds of higher trophic position are more efficient transferer (Michelutti et al., 2010) because
many pollutants become biomagnified through food webs. Pb level
does not show any substantial difference between emperor penguin
ornithogenic sediments PI and Pygoscelis penguin ornithogenic sediments Y2 (23.8 ± 1.7 mg kg− 1 vs. 15.7 ± 0.7 mg kg− 1, data from
this study and Sun and Xie, 2001), mainly because Pb is not
bioaccumulated through food chain (Sun and Xie, 2001). The concentration of Hg, however, increases in living organisms along the trophic
chain through bioaccumulation and biomagnification (Riisgard and
Hansen, 1990). The Hg level in PI is as high as 281 ± 25 ng g−1,
much higher than those in Adélie penguin ornithogenic sediments
from Ardley Island and Vestfold Hills (55 ± 2 ng g−1 (n = 46) and
10 ± 0.4 ng g−1 (n = 55), respectively) (Sun et al., 2006; Huang
et al., 2009a) and even those in pure Adélie penguin guanos from Ross
Island (150 ± 8 ng g−1, n = 3) (Nie et al., 2012). The great differences
in Hg concentration between Adélie and emperor penguin ornithogenic
sediments are mainly due to their different trophic positions. Unlike
Adélie penguins, which mainly feed on krill of lower trophic level, emperor penguins eat fishes of higher trophic level and occupy a higher
trophic position (Cherel, 2008). Because of their high transfer efficiency,
emperor penguins' role in transferring materials from ocean to land
should not be underestimated or even ignored, especially in the barren
Antarctic terrestrial systems, even though the population of juvenile
emperor penguins that visited on land is smaller than that of Adélie
penguins.
5. Conclusion
Based on stable isotope and elemental geochemical analyses on
two sediment cores EPI and PI from the N island near Amanda Bay,
we conclude that EPI is composed of natural freshwater algae sedimentation and PI is strongly influenced by emperor penguin guano
input. The Igeo values of elements in PI sediments show that emperor
penguins at Amanda Bay have significant impacts on local island and
pond systems. Juvenile emperor penguins transfer large amounts of
nutrients and contaminants from Southern Ocean to island environment,
and lead to substantial enrichment of Se, TP and Hg in lake sediments.
Though the population of emperor penguins that have direct impacts
on land systems is small, emperor penguins' role in the biogeochemical
cycle between ocean and land should not be ignored, especially in the
Antarctic land systems.
Conflict of interest
The authors declare no conflict of interests.
Acknowledgments
This study was funded by NSFC (Nos. 41106162 and 40730107), Chinese
Polar Environment Comprehensive Investigation & Assessment Programmes
(CHINARE2013-02-01-03, CHINARE2013-04-01-07 and CHINARE2013-0404-09) and the Central Universities (WK2080000017). Samples in this study
were provided by the BIRDS-Sediment system. We thank the Chinese Arctic
and Antarctic Administration and Polar Research Institute of China for logistical
support in field; Dr. Jie Tang and Changgui Lu provide help in field for samples
collection.
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