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Journal ArticleDOI

Investigation of mercury concentrations in fur of phocid seals using stable isotopes as tracers of trophic levels and geographical regions

13 Apr 2011-Polar Biology (Springer-Verlag)-Vol. 34, Iss: 9, pp 1411-1420

TL;DR: The results showed a positive correlation between Hg concentrations and δ15N values among all individuals and a trophic segregation was observed between crabeater seals and the other species, resulting from the very specific diet of krill of this species and leading to the lowest observed HG concentrations.

AbstractRecent studies have shown that the complementary analysis of mercury (Hg) concentrations and stable isotopic ratios of nitrogen (δ15N) and carbon (δ13C) can be useful for investigating the trophic influence on the Hg exposure and accumulation in marine top predators. In this study, we propose to evaluate the interspecies variability of Hg concentrations in phocids from polar areas and to compare Hg bioaccumulation between both hemispheres. Mercury concentrations, δ15N and δ13C were measured in fur from 85 individuals representing 7 phocidae species, a Ross seal (Ommatophoca rossii), Weddell seals (Leptonychotes weddellii), crabeater seals (Lobodon carcinophagus), harbour seals (Phoca vitulina), grey seals (Halichoerus grypus), ringed seals (Pusa hispida) and a bearded seal (Erignathus barbatus), from Greenland, Denmark and Antarctica. Our results showed a positive correlation between Hg concentrations and δ15N values among all individuals. Seals from the Northern ecosystems displayed greater Hg concentrations, δ15N and δ13C values than those from the Southern waters. Those geographical differences in Hg and stable isotopes values were likely due to higher environmental Hg concentrations and somewhat greater number of steps in Arctic food webs. Moreover, dissimilarities in feeding habits among species were shown through δ15N and δ13C analysis, resulting in an important interspecific variation in fur Hg concentrations. A trophic segregation was observed between crabeater seals and the other species, resulting from the very specific diet of krill of this species and leading to the lowest observed Hg concentrations.

Topics: Phoca (56%), Leptonychotes weddellii (53%)

Summary (2 min read)

Introduction

  • Mercury (Hg) is a global contaminant released into the ecosystem from both natural and anthropogenic sources (Pacyna et al. 2006).
  • Biological factors like age, sex or physiological status are known to influence the diet, and thereby, the exposure and accumulation of Hg in many species.
  • The underlying principle is that ratios of heavier vs lighter isotopes of nitrogen and carbon in tissues of predators can be traced to those of their prey as these two elements are assimilated through the diet.
  • In the Northern hemisphere, harbour and grey seals feed on a wide range of organisms, pelagic and benthic fish, cephalopods and crustaceans (Reeves et al. 1992).
  • Fur provides a non-invasive way to investigate metals and stable isotopes of seals.

Sampling procedure and preparation

  • Hair samples of 85 seals were obtained from seven phocid seal species, i.e. Length and weight of the animals were recorded, and age was estimated visually based on size and fur colour, according to three classes (yearling, juvenile and adult).
  • Subsequently, the hair samples were rinsed in several ultra-pure Milli-Q water baths, and dried for 24 hours at room temperature.
  • Analytical procedures, instrumentation and quality assurance for Hg measurements.
  • The analytical precision of the measurements was < 0.06‰ for carbon and < 0.1‰ for nitrogen, based on replicate measurements of acetanilide as internal laboratory reference material.

Statistical analysis

  • Prior to the statistical analyses, the Hg data were log-transformed (base e) to reduce skewness and fit parametric requirements.
  • Shapiro–Wilk and Bartlett test were applied to test the assumptions of parametric tests, such as analysis of variance and linear regression analysis.
  • In few cases, the assumptions were not fulfilled because of a couple of high Hg concentration values.
  • If the first runs of ANOVA test showed no significance of the interaction between two factors, the interaction factor was removed and the test re-run.
  • The number of individuals was low for some of the species, and only crabeater seals, Weddell seals and ringed seals were represented by more than 10 individuals (Table 1).

Influence of sex and age classes

  • Only adult individuals were selected to test the factor sex.
  • The three categories of age (yearling, juvenile and adult) were not all well represented for each species (Table 1).
  • Thus, the influence of sex on Hg concentrations was tested only on the crabeater seals, while the influence of age classes was tested on crabeater seals, Weddell seals and ringed seals.
  • Influence of the species and the geographical area 13 C values also varied among the species except for between ringed seals and grey seals (Table 2, Fig. 4B).

Influence of sex and age groups on Hg concentrations in fur

  • The influence of gender on Hg concentrations varies among studies and species.
  • Since δ 13 C values are generally greater in benthic or sea-ice algae than in pelagic algae (Fry and Sherr 1984; Tamelander et al. 2006), their results, with significantly lower δ.
  • 13 C values were observed between juvenile and adult individuals of ringed seals and Weddell seals, suggesting that juvenile seals of those species tend to explore different foraging habitats than the adults.
  • Thus, it would indicate a greater participation of the Northern species in the sympagic food web than the Southern ones.
  • Hg concentrations in adult harbour seals could result from that they feed on larger prey with greater burdens of Hg than ringed seal yearlings.

Conclusion

  • This demonstrates that fur is a good tissue for monitoring exposure to Hg in phocid seals and for reconstructing their exposure history through their diet, especially with the non-destructive and invasive sampling protocols relative to this tissue.
  • The comparison of both hemispheres showed the greater Hg concentrations in the Northern one, which would be the result of a greater contamination and /or somewhat longer food chains in the Arctic.
  • The use of these analytical tools contributes to a better understanding of local ecosystem functions permitting investigations of partitioning of habitat use and trophic levels of similar species co-existing within the same ecosystem.

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Investigation of mercury concentrations in fur of phocid
seals using stable isotopes as tracers of trophic levels
and geographical regions
Aurore Aubail, Jonas Teilmann, Rune Dietz, Frank Rigét, Tero Harkonen,
Olle Karlsson, Aqqalu Rosing-Asvid, Florence Caurant
To cite this version:
Aurore Aubail, Jonas Teilmann, Rune Dietz, Frank Rigét, Tero Harkonen, et al.. Investigation of
mercury concentrations in fur of phocid seals using stable isotopes as tracers of trophic levels and
geographical regions. Polar Biology, Springer Verlag, 2011, 34 (9), pp.1411-1420. �10.1007/s00300-
011-0996-z�. �hal-00611657�

1
Investigation of mercury concentrations in fur of phocid seals using stable isotopes as tracers
of trophic levels and geographical regions
Aurore Aubail
a, b,
*, Jonas Teilmann
a
, Rune Dietz
a
, Frank Rigét
a
, Tero Harkonen
c
, Olle Karlsson
c
,
Aqqalu Rosing-Asvid
d
, Florence Caurant
b
a
National Environmental Research Institute, Aarhus University, Frederiksborgvej 399, P.O. Box 358, DK-4000 Roskilde, Denmark
b
Littoral, Environnement et Sociétés (LIENSs), UMR 6250, CNRS-Université de La Rochelle, 2 rue Olympe de Gouges, F-17042 La
Rochelle cedex, France
c
Department of Contaminant Research, Swedish Museum of Natural History, P.O. Box 50007, S-10405 Stockholm, Sweden
d
Greenland Institute of Natural Resources, P.O. Box 570, 3900 Nuuk, Greenland
* Corresponding author:
E-mail address: aaubail@yahoo.fr
Tel.: +33 546507629; Fax.: +33 546458264

2
Abstract
Recent studies have shown that the complementary analysis of mercury (Hg) concentrations and
stable isotopic ratios of nitrogen (δ
15
N) and carbon (δ
13
C) can be useful for investigating the trophic
influence on the Hg exposure and accumulation in marine top predators. In this study, we propose
to evaluate the interspecies variability of Hg concentrations in phocids from polar areas and to
compare Hg bioaccumulation between both hemispheres. Mercury concentrations, δ
15
N and δ
13
C
were measured in fur from 85 individuals representing 7 phocidae species, a Ross seal
(Ommatophoca rossii), Weddell seals (Leptonychotes weddellii), crabeater seals (Lobodon
carcinophaga), harbour seals (Phoca vitulina), grey seals (Halichoerus grypus), ringed seals (Phoca
hispida), and a bearded seal (Erignathus barbatus), from Greenland, Denmark and Antarctica. Our
results showed a positive correlation between Hg concentrations and δ
15
N values among all
individuals. Seals from the Northern ecosystems displayed greater Hg concentrations, δ
15
N and δ
13
C
values than those from the Southern waters. Those geographical differences in Hg and stable
isotopes values were likely due to higher environmental Hg concentrations and somewhat greater
number of steps in Arctic food webs. Moreover, dissimilarities in feeding habits among species
were shown through δ
15
N and δ
13
C analysis, resulting in an important interspecific variation in fur
Hg concentrations. A trophic segregation was observed between crabeater seals and the other
species, resulting from the very specific diet of krill of this species and leading to the lowest
observed Hg concentrations.
Key words: Hg, nitrogen, carbon, hair, Arctic, Antarctica

3
Introduction
Mercury (Hg) is a global contaminant released into the ecosystem from both natural and
anthropogenic sources (Pacyna et al. 2006). The gaseous elemental form of this metal is very
volatile, and once in the atmosphere, it can be transported from mid to high latitudes over long
distances, and thereby reach the polar regions (Brooks et al. 2005). Although Hg is partly re-emitted
to the air, it is accumulated in organisms and biomagnified in the trophic chain in polar ecosystems
(Atwell et al. 1998; Bargagli et al. 1998). Thus, organisms feeding on species at high trophic levels
generally show greater Hg concentrations than those feeding on species at lower trophic levels.
Since marine mammals mainly are exposed to Hg through their diet (Aguilar et al. 1999),
differences in foraging strategies and feeding habits among species may lead to differences in
exposure to Hg, resulting in interspecific disparities in concentrations of Hg.
Biological factors like age, sex or physiological status are known to influence the diet, and thereby,
the exposure and accumulation of Hg in many species. However, differences in Hg concentrations
can also result from geographical or temporal variations in the environmental levels of Hg. Whether
differences in Hg concentrations among species result from differences in diet or environmental
levels of Hg can be investigated by analysing naturally occurring variations in stable isotopes of
nitrogen (
15
N and
14
N) and carbon (
13
C and
12
C) (Hobson and Welch 1992). The underlying
principle is that ratios of heavier vs lighter isotopes of nitrogen and carbon in tissues of predators
can be traced to those of their prey as these two elements are assimilated through the diet.
Consumer tissues are stepwise enriched in
15
N relative to those of their prey, and consequently,
δ
15
N measurements can be used to determine the trophic position of organisms (Minagawa and
Wada 1984). In contrast, δ
13
C values vary little through the food chain (<1‰), and can thus help to
determine the source of carbon used by primary consumers in a food web, and provide information
on the foraging habitat of the studied organisms (Fry and Sherr 1984). Furthermore, turn over rates
of stable isotopes in tissues vary with the metabolic rate of the tissue (Tieszen et al. 1983), and
isotopic analyses can give information on feeding habits over the last days, weeks, months or years,
depending on which tissue types are analysed.
Phocid seals are long-lived marine mammals at the top of food chains in polar ecosystems. Using
stable isotopes of nitrogen and carbon as tracers of the trophic level and habitat use respectively, we
investigated if concentrations of Hg in seal species from different geographical areas could be used
to determine the trophic levels they prey upon. We studied a Ross seal (Ommatophoca rossii),
Weddell seals (Leptonychotes weddellii) and crabeater seals (Lobodon carcinophaga) from

4
Antarctic regions, harbour seals (Phoca vitulina) and grey seals (Halichoerus grypus) found
throughout coastal regions of the Northern hemisphere, and ringed seals (Phoca hispida) and a
bearded seal (Erignathus barbatus), which both show Northern circumpolar distributions (Reeves et
al. 1992).
While the Ross seal has a varied diet based on squid, fish and krill, and the Weddell seal mainly
feeds on fish, but also on various cephalopods and crustaceans, the crabeater seal is specialised on
feeding almost exclusively on Antarctic krill (Bowen et al. 2002). In the Northern hemisphere,
harbour and grey seals feed on a wide range of organisms, pelagic and benthic fish, cephalopods
and crustaceans (Reeves et al. 1992). Finally, ringed seals are believed to feed mainly on a variety
of fish and invertebrates such as amphipods, euphausiids and cephalopods, while the bearded seal
consumes mainly benthic invertebrates, i.e. clams, crustaceans, cephalopods as well as some fish
(Reeves et al. 1992). Pauly et al. (1998) estimated the trophic levels of several marine mammals
mainly by stomach content analysis. Values for trophic levels ranged from 3.3 for the crabeater seal
to 4.1 for the Ross seal. Estimated values were 3.4 for bearded seals, 3.8 for ringed seals, harbour
seals and grey seals, whereas it was estimated at 4.0 for Weddell seals.
Soft tissues are commonly used for analysis of metals and stable isotopes. However, fur provides a
non-invasive way to investigate metals and stable isotopes of seals. Fur is keratin-based containing
records of metallic and isotopic elements which are deposited there during the annual moult.
Mercury is one of the trace elements transported to the fur follicles via the blood supply (Ikemoto et
al. 2004), and subsequently incorporated into the hair during periods of growth (Brookens et al.
2007). Hair is widely used as an indicator of blood Hg levels for mammals, and particularly for
humans, and has been used as an indicator of exposure to the environmental pollution also in
pinnipeds (Brookens et al. 2007; Gray et al. 2008; Ikemoto et al. 2004; Medvedev et al. 1997;
Watanabe et al. 1996; Wenzel et al. 1993; Yamamoto et al. 1987).
The purpose of this study was to determine Hg concentrations in the fur of seven species of phocid
seals from different geographical areas, and to evaluate the influence of biological factors in the
bioaccumulation process. Stable isotope analyses were used to evaluate differences or similarities in
the diet or in the foraging habitat among species that could explain variations in Hg concentrations.
We also evaluated if fur can be used for monitoring of Hg in phocid seals in the future.

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  • ...Previous studies on Arctic ecosystems have already shown that Hg analyses coupled to δ15N (e.g. Atwell et al., 1998) or both δ13C and δ15N (e.g. Aubail et al., 2011) allows a better understanding of Hg biomagnification pathways and moreover, the influence of feeding ecology factors such as change…...

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Abstract: In the present work, fat, skin, liver and muscle samples from Leptonychotes weddellii (Weddell seal, n = 2 individuals), Lobodon carcinophagus (crabeater seal, n = 2), Arctocephalus gazella (Antarctic fur seal, n = 3) and Mirounga leonina (southern elephant seal, n = 1) were collected from King George Island, Antarctica, and analysed for POPs (PCBs, organochlorine pesticides and PBDEs) and stable isotopes (δ13C and δ15N in all tissues but fat). PBDEs could be found in only one sample (L. weddellii fat). Generally, PCBs (from 74 to 523 ng g−1 lw), DDTs (from 14 to 168 ng g−1 lw) and chlordanes (from 9 to 78 ng g−1 lw) were the prevailing compounds. Results showed a clear stratification in accordance with ecological data. Nonetheless, stable isotope analyses provide a deeper insight into fluctuations due to migrations and nutritional stress. Correlation between δ15N and pollutants suggests, to some degree, a considerable ability to metabolize and/or excrete the majority of them.

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Cites background from "Investigation of mercury concentrat..."

  • ...For comparison purposes, the closest trophic equivalent to L. weddellii in the northern hemisphere would be the grey seal, Halichoerus grypus, with the closest (yet slightly higher) d15N (data from Aubail et al., 2011)....

    [...]

  • ...This is specially the case for L. carcinophagus, which feed on krill, Euphausia superba, practically all year round (Berta et al., 2006)....

    [...]

  • ...Another reason might be that food chains in the Arctic are somewhat longer than in the Antarctic (Aubail et al., 2011)....

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Abstract: The massive number of seabirds (penguins and procellariiformes) and marine mammals (cetaceans and pinnipeds) - referred to here as top predators - is one of the most iconic components of the Antarctic and Southern Ocean. They play an important role as highly mobile consumers, structuring and connecting pelagic marine food webs and are widely studied relative to other taxa. Many birds and mammals establish dense breeding colonies or use haul-out sites, making them relatively easy to study. Cetaceans, however, spend their lives at sea and thus aspects of their life cycle are more complicated to monitor and study. Nevertheless, they all feed at sea and their reproductive success depends on the food availability in the marine environment, hence they are considered useful indicators of the state of the marine resources. In general, top predators have large body sizes that allow for instrumentation with miniature data-recording or transmitting devices to monitor their activities at sea. Development of scientific techniques to study reproduction and foraging of top predators has led to substantial scientific literature on their population trends, key biological parameters, migratory patterns, foraging and feeding ecology, and linkages with atmospheric or oceanographic dynamics, for a number of species and regions. We briefly summarize the vast literature on Southern Ocean top predators, focusing on the most recent syntheses. We also provide an overview on the key current and emerging pressures faced by these animals as a result of both natural and human causes. We recognize the overarching impact that environmental changes driven by climate change have on the ecology of these species. We also evaluate direct and indirect interactions between marine predators and other factors such as disease, pollution, land disturbance and the increasing pressure from global fisheries in the Southern Ocean. Where possible we consider the data availability for assessing the status and trends for each of these components, their capacity for resilience or recovery, effectiveness of management responses, risk likelihood of key impacts and future outlook.

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References
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Abstract: The isotopic composition of nitrogen was measured in marine and fresh-water animals from the East China Sea, The Bering Sea, Lake Ashinoko and Usujiri intertidal zone. Primary producers, showed average δ15Nversus atmospheric nitrogen of +5.0%. (+3.4 to +7.5) in the Bering Sea and Lake Ashinoko, and +6.8%. (+6.0 to +7.6) in Usujiri intertidal zone. Blue green algae from the East China Sea show an average −0.55%. (−0.8 to +1.2). All consumers, Zooplankton, fish and bird exhibited Stepwise enrichment of 15N with increasing trophic level. The 15N enrichment at a single feeding process ranged from +1.3 to +5.3 averaging +3.4 ± 1.1%.. This isotopic fractionation seems to be independent of habitat. The effect of age in animals was obtained by analyzing two marine mussels. The soft tissue nitrogen showed +2.0%. enrichment relative to that of primary producers, and the magnitude was almost constant with shell ages ranging from 0 to 8 years. A similar 15N enrichment occurs in all Molluscs, Crustaceans, Insecta, Amphibia, Fish, Ave and Mammal species regardless of the difference in the form of excreted nitrogen and in laboratory cultured fish, brine shrimp and mice (+2.9 to +4.9%.). The excreted ammonia from guppy was sufficiently light to balance the concentration of 15N to animal body.

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"Investigation of mercury concentrat..." refers background in this paper

  • ...Consumer tissues are stepwise enriched in 15N relative to those of their prey, and consequently, d15N measurements can be used to determine the trophic position of organisms (Minagawa and Wada 1984)....

    [...]

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"Investigation of mercury concentrat..." refers background or result in this paper

  • ...In contrast, d(13)C values vary little through the food chain (\1%) and can thus help to determine the source of carbon used by primary consumers in a food web and provide information on the foraging habitat of the studied organisms (Fry and Sherr 1984)....

    [...]

  • ...%) and can thus help to determine the source of carbon used by primary consumers in a food web and provide information on the foraging habitat of the studied organisms (Fry and Sherr 1984)....

    [...]

  • ...Since d(13)C values are generally greater in benthic or sea-ice algae than in pelagic algae (Fry and Sherr 1984; Tamelander et al. 2006), our results, with significantly lower d(13)C values in the juveniles, suggest that juvenile individuals may forage mainly krill in the water column....

    [...]

  • ...Since d13C values are generally greater in benthic or sea-ice algae than in pelagic algae (Fry and Sherr 1984; Tamelander et al. 2006), our results, with significantly lower d13C values in the juveniles, suggest that juvenile individuals may forage mainly krill in the water column....

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TL;DR: It is shown that tissues of the gerbil have different δ13C values when equilibrated on corn (C4) or wheat (C3) diets with constant 13C/12C contents, which has important implications for the use of δ 13C values as indicators of animal diet.
Abstract: The use of stable carbon isotopes as a means of studying energy flow is increasing in ecology and paleo- ecology. However, secondary fractionation and turnover of stable isotopes in animals are poorly understood pro- cesses. This study shows that tissues of the gerbil (Meriones unguienlatus) have different 613C values when equilibrated on corn (C4) or wheat (C~) diets with constant 13c/1ac contents. Lipids were depleted 3.0%o and hair was enriched 1.0%o relative to the C4 diet. Tissue 6t3C values were ranked hair > brain > muscle > liver > fat. After changing the gerbils to a wheat (C3) diet, isotope ratios of the tissues shifted in the direction of the 6a3C value of the new diet. The rate at which carbon derived from the corn diet was replaced by carbon derived from the wheat diet was ade- quately described by a negative exponential decay model for all tissues examined. More metabolically active tissues such as liver and fat had more rapid turnover rates than less metabolically active tissues such as hair. The half-life for carbon ranged from 6.4 days in liver to 47.5 days in hair. The results of this study have important implications for the use of 6~3C values as indicators of animal diet. Both fractionation and turnover of stable carbon isotopes in animal tissues may obscure the relative contributions of isotopically distinct dietary components (such as C3 vs. C,, or marine vs. terrestrial) if an animal's diet varies through time. These complications deserve attention in any study using stable isotope ratios of animal tissue as dietary indicators and might be minimized by analysis of several tissues or products covering a range of turnover times.

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"Investigation of mercury concentrat..." refers background in this paper

  • ...Furthermore, turnover rates of stable isotopes in tissues vary with the metabolic rate of the tissue (Tieszen et al. 1983), and isotopic analyses can give information on feeding habits over the last days, weeks, months or years, depending on which tissue types are analysed....

    [...]


Journal ArticleDOI

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"Investigation of mercury concentrat..." refers background in this paper

  • ...Whether differences in Hg concentrations among species result from differences in diet or environmental levels of Hg can be investigated by analysing naturally occurring variations in stable isotopes of nitrogen ((15)N and (14)N) and carbon ((13)C and (12)C) (Hobson and Welch 1992)....

    [...]

  • ...Whether differences in Hg concentrations among species result from differences in diet or environmental levels of Hg can be investigated by analysing naturally occurring variations in stable isotopes of nitrogen (15N and 14N) and carbon (13C and 12C) (Hobson and Welch 1992)....

    [...]


Frequently Asked Questions (1)
Q1. What are the contributions in "Investigation of mercury concentrations in fur of phocid seals using stable isotopes as tracers of trophic levels and geographical regions" ?

Aail et al. this paper used stable isotopes of nitrogen and carbon as tracers of the trophic level and habitat use respectively.