Hg stable isotope variations in marine top ... - ACS Publications

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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

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ACS Earth and Space Chemistry

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Hg stable isotope variations in marine top

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predators of the Western Arctic Ocean

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

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Point*1

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

Observatoire

Midi-Pyrénées,

Laboratoire

Géosciences

Environnement

Toulouse,

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2

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

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3

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

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Rochelle, France

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

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RECEIVED DATE

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

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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

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Abstract

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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Arctic Ocean before entering the marine food web.

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

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Introduction

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

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

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

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

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

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

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of unique atmospheric Hg depositional conditions and springtime primary production have

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

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

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

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

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

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inorganic Hg emission and MMHg bioaccumulation have been proposed

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

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undoubtedly, the most dramatic physical change

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

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

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13

7-11

2, 12

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causing

. The various

. In particular,

. Ringed seals, beluga whales and polar

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

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biogeochemical, ecological and metabolic factors behind MMHg exposure

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

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reactions

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

. Mass

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

3 ACS Paragon Plus Environment


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

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work did document intracellular MIF during photomicrobial MMHg breakdown and inorganic

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Hg reduction

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photochemical MMHg Δ199Hg composition behaves conservatively up the food chain

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

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

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

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studies have discussed sea-ice control on geographical

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observed in various Alaskan bioindicators.

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

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and temporal

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23, 24

.

MIF variation

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

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

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

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

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

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foodweb data

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

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

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

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cycling across the N-Pacific – Arctic Ocean continuum.

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Materials and methods

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Sampling

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

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

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

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

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

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

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25

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Toulouse laboratory until analysis.

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. 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

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

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

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

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

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

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

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

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samples coming from a common location.

.

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

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

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

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

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

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

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



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Analysis

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

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

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fractions (preparation detailed in the SI,

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

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

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

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

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

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

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

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

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

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were determined by isotope dilution gas chromatography inductively coupled plasma mass

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

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derivatization at the IPREM laboratory (Pau, France)

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measurement accuracy are presented in previous works 23, 28.

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) by Elemental Analysis - Isotope Ratio Mass

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. Details of the method and

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

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

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

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

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

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sample-standard bracketing according to the following equation:


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(1) δ

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Hg(‰) =

− 1" × 1000

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where xxx represents the mass of each mercury isotope

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

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

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

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

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

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

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

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

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between 1 to 4 times.

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Long term reproducibility between the different series of experiments was evaluated

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

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Measurements performed at different concentration levels were highly consistent in terms

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of precision and accuracy (Table S-2,

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

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

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other published values (Table S-2)

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

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

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. Uncertainties applied to samples were the larger of



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Statistics

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

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

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

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

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

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Marine mammal ecology

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Beluga foraging ecology and migration routes

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

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seasonal migrations

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

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four stocks.

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. The comparison of ecological and satellite telemetry studies with

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

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

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

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

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

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

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

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

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

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

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

. This is the 30

. The


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

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habitat

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

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

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

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

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

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

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

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Amundsen Gulf ) in summer

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

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

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Ringed seals vs polar bears trophic relationship

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. Following this temporary summer coastal habitat, satellite telemetry studies

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

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

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

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

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content analysis

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restrained habitat in the shore zone (

Hg stable isotope variations in marine top ... - ACS Publications

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