Hg-Stable Isotope Variations in Marine Top Predators of the Western

Subscriber access provided by UNIV OF DURHAM

Hg stable isotope variations in marine top predators of the Western Arctic Ocean Jeremy Masbou, Jeroen E. Sonke, David Amouroux, Gaël Guillou, Paul R. Becker, and David Point ACS Earth Space Chem., Just Accepted Manuscript • DOI: 10.1021/ acsearthspacechem.8b00017 • Publication Date (Web): 23 Apr 2018 Downloaded from http://pubs.acs.org on April 24, 2018

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Earth and Space Chemistry

1

Hg stable isotope variations in marine top

2

predators of the Western Arctic Ocean

3 4

Jérémy Masbou*1, Jeroen E. Sonke1, David Amouroux2, Gaël Guillou3, Paul R. Becker4, David

5

Point*1

6 7 8

1

9

CNRS/IRD/Université Paul Sabatier Toulouse 3, 14 avenue Edouard Belin, 31400 Toulouse,

Observatoire

Midi-Pyrénées,

Laboratoire

Géosciences

Environnement

Toulouse,

10

2

11

pour l'Environnement et les Materiaux , UMR5254, 64000, Pau, France

12

3

13

Rochelle, Institut du Littoral et de l’Environnement, 2 rue Olympe de Gouges, 17000 La

14

Rochelle, France

15

4

16

Marine Laboratory, 331 Fort Johnson Road, Charleston, South Carolina 29412 USA.

17

RECEIVED DATE

18

*Authors for correspondence: [email protected], [email protected]

19

CNRS/ UNIV PAU & PAYS ADOUR, Institut des Sciences Analytiques et de Physico-chimie

UMR Littoral, Environnement et Sociétés (LIENSs), UMR 7266 CNRS-Université de La

National Institute of Standards and Technology, Analytical Chemistry Division, Hollings

Phone: +33 (0)5 61 33 26 06 1 ACS Paragon Plus Environment

ACS Earth and Space Chemistry 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

20

Page 2 of 37

Abstract

21

Recent studies on mercury (Hg) stable isotopes in Alaskan seabird eggs and ringed

22

seal livers illustrated the control of sea ice cover on marine methyl-Hg photochemistry. Here,

23

complementary marine mammal tissues have been analyzed to document variations in Hg,

24

carbon (C), and nitrogen (N) stable isotope compositions of Arctic marine food webs.

25

Mercury stable isotope ratios were measured in liver samples of 55 beluga whales

26

(Delphinapterus leucas) and 15 polar bears (Ursus maritimus) collected since 1990. Large

27

variations in δ202Hg (≈2.1‰) and Δ199Hg (≈1.7‰) are observed between species and within

28

species stocks covering the Gulf of Alaska – Bering Sea – Arctic Ocean regions. Polar bears,

29

mainly feeding on ringed seal (δ15N shift of 4.2‰), show identical liver Δ199Hg of 0.5‰,

30

confirming the absence of metabolic mass independent fractionation, and 0.33±0.11‰

31

enrichment in heavy Hg isotopes. Beluga whale liver total Hg concentrations increase with

32

age, reflecting lifetime bioaccumulation, while Hg speciation shifts to inorganic Hg with age

33

due to hepatic methyl-Hg breakdown. Δ200Hg variations in biota show a small, 0.1‰

34

decrease from North-Pacific Ocean to Arctic Ocean habitats, suggesting atmospheric Hg

35

deposition to be important in the Pacific, and terrestrial Hg inputs to dominate in the Arctic

36

Ocean. Similar to seabird eggs, a consistent south to north gradient in Δ199Hg baseline is seen

37

in mammal liver tissues, confirming sea ice cover as a control factor on marine Hg

38

photoreduction and Δ199Hg. Arctic Ocean beluga whales have near zero Δ199Hg indicating

39

that terrestrial Hg and in situ produced methyl-Hg are not measurably photoreduced in the

40

Arctic Ocean before entering the marine food web.

41 42

KEYWORDS: ARCTIC, MERCURY, ISOTOPES, MIF, MAMMALS 2 ACS Paragon Plus Environment

Page 3 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


43

Introduction

44

Mercury (Hg) in the Arctic has become a serious concern since the discovery of

45

elevated mercury concentration in biota 1, contradicting its status as a pristine ecosystem. In

46

particular, the neurotoxic monomethyl-Hg (MMHg) form of Hg is known to biomagnify and

47

bioaccumulate in marine food webs. Situated at the top of the food chain, Arctic marine

48

mammals exhibit some of the highest tissue Hg concentrations in the world

49

adverse health effects in northern people consuming them 3, 4. The simultaneous occurrence

50

of unique atmospheric Hg depositional conditions and springtime primary production have

51

long been thought to be responsible for enhanced production of bio-available MMHg 5, 6. Yet

52

the dominant site(s) of inorganic Hg (iHg) methylation (e.g. coastal sediments, cryosphere,

53

marine water column) in the Arctic marine ecosystem are not well known

54

geographical and temporal trends observed in biota suggest a complex picture of the Arctic

55

bio-geochemical Hg cycle 4. Climate-related variables occurring between the moment of

56

inorganic Hg emission and MMHg bioaccumulation have been proposed

57

the extensive loss of sea ice which has occurred over recent decades in the Arctic region is,

58

undoubtedly, the most dramatic physical change

59

bears live in close association with sea ice and are therefore sensitive bioindicators for

60

detecting modifications in climate change related MMHg exposure 14, 15.

61

13

7-11

2, 12

2

causing

. The various

. In particular,

. Ringed seals, beluga whales and polar

Mercury stable isotope compositions of biota tissues contain information on the 16, 17

62

biogeochemical, ecological and metabolic factors behind MMHg exposure

63

dependent Hg isotope fractionation (MDF, δ202Hg) is observed during both abiotic and biotic

64

reactions

65

predominantly during extracellular photo-induced reactions such as inorganic Hg photo-

. Mass

18, 19

. Large mass independent Hg isotope fractionation (MIF, Δ199Hg) occurs

3 ACS Paragon Plus Environment


Page 4 of 37

66

reduction or MMHg photo-demethylation in aqueous media prior to bio-uptake 20, 21. Recent

67

work did document intracellular MIF during photomicrobial MMHg breakdown and inorganic

68

Hg reduction

69

photochemical MMHg Δ199Hg composition behaves conservatively up the food chain

70

The Δ199Hg magnitude in mammal tissues can then be used to quantify photoreduction

71

conditions in the aquatic ecosystem or to understand prey-predator relationships. Since sea

72

ice cover acts as a physical layer between ocean and atmosphere, two of our previous

73

studies have discussed sea-ice control on geographical

74

observed in various Alaskan bioindicators.

22

. With the absence of MIF during biotic processes in higher animals, the

16

and temporal

23

23, 24

.

MIF variation

75

In this study, we complement the Arctic bioindicator dataset with the Hg isotope

76

compositions of 55 beluga whale and 15 polar bear liver tissues collected at different

77

Alaskan locations. Additional parameters such as Hg speciation and δ13C and δ15N allow for

78

the comparison of the metabolic and ecological patterns among the bioindicators.

79

Combining the whole arctic biomonitor dataset (>200 samples, four species), N-Pacific

80

foodweb data

81

objectives of this study are i) to trace metabolic/ecological processes that influence Hg

82

isotope composition, ii) to trace Hg processes (e.g. photodegradation) and sources (oceanic

83

vs. terrestrial) before it is incorporated into the marine arctic food web, iii) to understand Hg

84

cycling across the N-Pacific – Arctic Ocean continuum.

85

Materials and methods

86

Sampling

17

and other Hg isotope data (rainfall, snowfall, soils, sediments…), the

87

Beluga whale and polar bear liver samples originate from the Alaska Marine Mammal

88

Tissue Archival Project (AMMTAP). The tissues were sampled by Alaskan native subsistence 4 ACS Paragon Plus Environment

Page 5 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


89

hunters and were homogenized and archived under cryogenic conditions by the National

90

Bio-monitoring Specimen Bank (NBSB) located at the National Institute of Standard and

91

Technology (NIST, Charleston, SC). Standard preparation protocols are described elsewhere

92

25

93

Toulouse laboratory until analysis.

94

. Samples were shipped frozen and stored at -80°C at the Geosciences Environnement

In this study, liver samples of 55 beluga whales (BW) and 15 polar bears (PB) were 23

95

analyzed and data from 53 ringed seals (RS) from our previous study were considered

96

Liver samples were chosen due to their large geographical/temporal coverage and their

97

availability compared to other tissues/organs, allowing for more powerful statistics. For all

98

specimens, the sampling period is from 1988 to 2002, and sampling locations are shown in

99

Figure 1. Beluga whale samples are from five different locations. From North to South,

100

Barrow (n=4), Point Lay (n=25), Point Hope (n=4), Norton Sound (n=4) and Cook Inlet (n=17).

101

For each location, no significant temporal trends were detected. We therefore pooled

102

samples coming from a common location.

.

103

Ringed seal samples originate from two different locations which are Barrow (n=39)

104

and Nome (n=14). Polar bear samples have mostly been sampled in Barrow (n=10), but

105

additional samples from Gambell, Little Diomede, Point Lay, Prudhoe Bay and Savoonga with

106

one sample at each location were also included. For clarity these locations have not been

107

included in Figure 1, but they are indicated in Figure S-1. Specimen details such as sex, length

108

and weight were determined on-site. Age determination was subsequently made on 24 BW,

109

9 PB and 48 RS by counting visible teeth or claw growth layer rings.



110

Page 6 of 37

Analysis

111

All preparation and analysis protocols have been detailed in the previous publication 23.

112

Briefly, carbon (δ13C) and nitrogen (δ15N) isotope ratios were measured on defatted sample

113

fractions (preparation detailed in the SI,

114

Spectrometry (EA-IRMS) at the Institut du Littoral et de l’Environnement (La Rochelle,

115

France). External instrument reproducibility for δ13C and δ15N is typically ±0.1‰. Total

116

mercury concentration (HgT, expressed on a wet weight basis) of fresh frozen samples was

117

determined in triplicate by atomic absorption after combustion and gold trapping using a

118

DMA-80 analyzer (Milestone, USA) at the GET laboratory. Accuracy was checked against

119

reference material: NRCC-DORM-2 (dry dogfish muscle), NIST-SRM 1947 (fresh-frozen trout

120

tissue) and a similar in-house matrix reference material: NIST QC03LH03 (whale liver control

121

material). Mercury concentrations of reference materials were not statistically different

122

from the certified values (Table S-1). Mercury speciation measurements on selected samples

123

were determined by isotope dilution gas chromatography inductively coupled plasma mass

124

spectrometry (ID-GC-ICPMS) following microwave-assisted extraction and aqueous phase

125

derivatization at the IPREM laboratory (Pau, France)

126

measurement accuracy are presented in previous works 23, 28.

26

) by Elemental Analysis - Isotope Ratio Mass

27

. Details of the method and

127

Mercury isotope compositions were measured at the Observatoire Midi-Pyrenees using

128

multi-collector inductively coupled plasma mass spectrometry (MC-ICP-MS; Thermo Finnigan

129

Neptune) with continuous flow cold vapour (CV) generation using Sn(II) reduction (CETAC

130

HGX-200). Mercury isotope composition is expressed in δ notation and reported in parts per

131

thousand (‰) deviation from the NIST SRM 3133 standard, which was determined by

132

sample-standard bracketing according to the following equation:


Page 7 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(1) δ

133

Hg(‰) =

− 1" × 1000

134

where xxx represents the mass of each mercury isotope

135

δ202Hg characterizes the mass dependent isotope fractionation (MDF) while mass

136

independent isotope fractionation (MIF) is expressed by the ∆ notation:

137

(2) ∆ +,,Hg(‰) = δ +,,Hg − (δ )*)Hg × 0.252)

(3) ∆ )**Hg(‰) = δ )**Hg − (δ )*)Hg × 0.502)

138 139

(4) ∆ )*+Hg(‰) = δ )*+Hg − (δ )*)Hg × 0.752)

140

Sample preparation is detailed in the SI. Final analyzed solutions containing between 1 to

141

5 ng Hg.g-1 and matching NIST 3133 concentrations within 15% were analyzed by CV-MC-ICP-

142

MS. Depending on the sample mass available, sample measurements were replicated

143

between 1 to 4 times.

144

Long term reproducibility between the different series of experiments was evaluated

145

with the matrix-matched whale liver NIST QC03LH03 in-house control material.

146

Measurements performed at different concentration levels were highly consistent in terms

147

of precision and accuracy (Table S-2,

148

(2SD, n=31) was observed for δ202Hg and ∆199Hg respectively. Secondary reference material

149

UM-Almaden was also analyzed, with δ202Hg values of -0.53±0.10‰ (2SD, n=46) consistent

150

other published values (Table S-2)

151

either the 2SD on the QC03LH03 control material or the 2SD on sample replicates.

23

). A long-term reproducibility of 0.14‰ and 0.11‰

20

. Uncertainties applied to samples were the larger of



152

Page 8 of 37

Statistics

153

Statistical analyses were performed using JMP® software (SAS Institute, USA). One-way

154

ANOVA tests were performed when comparing two datasets. Homogeneity of variances was

155

tested using the Brown-Forsythe test. In the case of unequal variances, a Welch ANOVA test

156

was used. For slope comparison, Real Statistics Resource Pack for Microsoft Excel® provided

157

by http://www.real-statistics.com was used.

158

Marine mammal ecology

159

Beluga foraging ecology and migration routes

160

Alaskan BW are distributed into five stocks with common genetic material and 29-31

161

seasonal migrations

162

the date and the sampling location allows us to classify individuals investigated here into

163

four stocks.

164

. The comparison of ecological and satellite telemetry studies with

Firstly, the Cook Inlet Stock (CI) is well defined because of the permanent occurrence 32

165

of the same group of beluga whales in the estuary without annual migration

166

most genetically distinct group and potential exchange with other stocks is limited

167

second stock is the East Bering Sea Stock (EBS) composed of samples obtained in the Norton

168

Sound summer aggregation area (64°N). Despite the lack of ecological studies for this stock,

169

their overwintering ground appears to cover the mid/south Bering Sea over the Bering Sea

170

shelf between 58-60°N. Thirdly, the East Chukchi Sea stock (ECS) is well documented and

171

composed of samples obtained at Point Lay and Barrow. Beluga whales from this stock

172

overwinter in the northern Bering Sea and tend to follow the coast up north in spring until

173

Barrow and Point Lay where they have been observed raising their calves and molting in the

174

coastal zone 33. Studies indicate that stomach contents are empty at spring suggesting that

. This is the 30

. The


Page 9 of 37 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


175

they do not feed in winter time and much Hg exposure likely reflects feeding in the summer

176

habitat

177

indicate that ECS belugas move up north to Barrow foraging intensively at the Beaufort shelf

178

break and in Barrow’s canyon (juveniles and adults). However, mature males and females

179

tend to feed much more offshore and deeply (200-1000m) in the open Chukchi sea and

180

Beaufort sea under dense sea ice conditions (>90%) 34. Finally, despite the southern sampling

181

location, BW from Point Hope belong to a fourth stock, the East Beaufort Sea stock (EBfS). It

182

is documented that BW from EBfS overwinter in the northern Bering Sea and pass Point

183

Hope in early spring to reach their Beaufort Sea habitat (Mackenzie River delta and

184

Amundsen Gulf ) in summer

185

Hope are consistent with this route. The separation between the different BW stocks is

186

evidenced by their unique δ13C vs δ15N combinations (Figure S-2).

187

Ringed seals vs polar bears trophic relationship

188

33

. Following this temporary summer coastal habitat, satellite telemetry studies

35, 36

. The early sampling dates (May 19th to May 26th) at Point

Barrow and Nome RS foraging behavior has been described in a previous publication

189

23

190

items which consist of a mix of fish (polar cod, pacific sand lace) and crustaceans

191

(euphausiacea, mysidacea, zooplancton, amphipoda, northern shrimp) according to stomach

192

content analysis

193

restrained habitat in the shore zone (

Hg-Stable Isotope Variations in Marine Top Predators of the Western

Recommend Documents