Environmental Origins of Methylmercury in Aquatic Biota and Humans

122 Pages·2017·11.9 MB·English

Environmental Origins of Methylmercury in Aquatic
Biota and Humans
Citation
Li, Miling. 2016. Environmental Origins of Methylmercury in Aquatic Biota and Humans. Doctoral
dissertation, Harvard T.H. Chan School of Public Health.
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http://nrs.harvard.edu/urn-3:HUL.InstRepos:27201754
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Dissertation Advisor: Dr. Elsie Sunderland Miling Li
Environmental Origins of Methylmercury in Aquatic Biota and Humans
Abstract
Methylmercury (MeHg) is a neurotoxin found in fish and shellfish, that poses risks to
human and ecological health. Exposure to MeHg adversely affects neurodevelopment of children
and cardiovascular health in adults. Seafood consumption is the primary exposure route to MeHg
in North America. An understanding of the link between environmental MeHg sources and
human exposures is needed to determine the impacts of ongoing environmental change.
However, few data exist for relating environmental exposures to human health outcomes.
Imprecision in dietary recall data on fish consumption and variability in MeHg concentrations
within and across seafood species consumed have made it challenging to accurately identify
sources of human MeHg exposure. In addition, the diverse environmental sources of MeHg
production in ecosystems make it more difficult to quantitatively attribute human exposures to
specific environments where methylation is taking place.
My doctoral dissertation uses naturally occurring mercury (Hg) stable isotopes to
characterize sources of MeHg exposure in aquatic biota and human populations. The objectives
of my work are to (1) explore the utility of Hg stable isotopes in human hair as a novel method
for tracing sources of MeHg exposure to humans; (2) examine drivers of the internal body
burden of MeHg in frequent seafood consumers; (3) refine understanding of environmental
MeHg sources for estuarine fish.
My first dissertation chapter characterizes the magnitude of mass-dependent fractionation
between seafood and consumers and shows Hg stable isotopes in human hair is a promising tool
ii
for estimating different Hg exposure sources (e.g., coastal vs. oceanic fish). My second chapter
uses dietary survey data and Hg isotopes in hair from high-frequency seafood consumers to show
that differences in in vivo demethylation do not explain variability in biomarker concentrations.
I infer that absorption efficiencies for MeHg in seafood are very low for some high-frequency
fish consumers and hypothesize that this is caused by interactions with co-ingested foods. The
last chapter investigates diverse Hg stable isotope signatures in benthic, riverine and pelagic
estuarine fish and uses these signatures to better characterize the relative importance of different
environmental MeHg sources.

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Table of Content
Abstract ........................................................................................................................................... ii
List of Figures ................................................................................................................................ vi
List of Tables ............................................................................................................................... viii
Acknowledgement ......................................................................................................................... ix
Chapter 1. Overview ....................................................................................................................... 1
1.1 Sources of mercury ............................................................................................................... 1
1.2 Hg stable isotope ratios ......................................................................................................... 2
1.3 Use of Hg stable isotopes to determine MeHg sources and processes ................................. 4
Chapter 2. Assessing sources of human methylmercury exposure using stable mercury isotopes
*....................................................................................................................................................... 7
Abstract ........................................................................................................................................... 7
2.1 Introduction ....................................................................................................................... 8
2.2 Methods ........................................................................................................................... 10
2.2.1 Sample collection: Faroe Islands ............................................................................... 10
2.2.2 Sample collection: Gulf of Mexico ........................................................................... 11
2.2.3 Hg stable isotope analyses ......................................................................................... 12
2.2.4 Data analysis and isotope mixing model ................................................................... 13
2.3 Results ............................................................................................................................. 14
2.3.1 Mass-independent fractionation in hair and seafood ................................................. 14
2.3.2 Mass-dependent fractionation in hair and seafood .................................................... 17
2.3.3 MeHg exposure sources calculated from hair Hg isotopes ....................................... 18
2.4 Discussion ........................................................................................................................ 20
2.4.1 Utility of Hg isotopes for tracking sources of MeHg ................................................ 20
2.4.2 Diverse MeHg sources in consumed fish .................................................................. 22
Supplemental materials ................................................................................................................. 26
Chapter 3. Insights from mercury stable isotopes into factors affecting the internal body burden
of methylmercury in frequent fish consumers* ............................................................................ 34
Abstract ......................................................................................................................................... 34
3.1 Introduction ..................................................................................................................... 36
3.2 Methods ........................................................................................................................... 38
3.2.1 Study population ....................................................................................................... 38
3.2.2 Hair total mercury analysis ....................................................................................... 40
3.2.3 MeHg intake and conversion to hair Hg equivalent .................................................. 40
3.2.4 Statistical predictors of hair Hg biomarkers .............................................................. 42
3.3 Results and discussion ..................................................................................................... 44
3.3.1 Comparison of external and internal Hg exposures .................................................. 44
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3.3.2 Variability in exposures due to fish MeHg and pharmacokinetics ........................... 46
3.3.3 Evaluation of dietary recall data using hair Hg isotope signatures ........................... 48
3.3.4 Mass-dependent fractionation of Hg isotopes as an indicator of MeHg demethylation
51
3.3.5 Variable absorption efficiency for MeHg ................................................................. 52
3.4 Conclusion ....................................................................................................................... 54
Supplemental materials ................................................................................................................. 58
Chapter 4. Environmental Origins of Methylmercury Accumulated in Subarctic Estuarine Fish
Indicated by Hg Stable Isotopes ................................................................................................... 65
Abstract ......................................................................................................................................... 65
4.1 Introduction ..................................................................................................................... 66
4.2 Methods ........................................................................................................................... 69
4.2.1 Sample collection ...................................................................................................... 69
4.2.2 Fish species age, habitat and diet classification ........................................................ 69
4.2.3 Total Hg and MeHg analysis ..................................................................................... 70
4.2.4 Carbon and nitrogen isotope analysis ........................................................................ 71
4.2.5 Hg stable isotope analysis ......................................................................................... 71
4.2.6 Data analysis ............................................................................................................. 73
4.3 Results ............................................................................................................................. 73
4.3.1 Fish habitats and hypothesized MeHg sources ......................................................... 73
4.3.2 Fish and sediment Hg isotopic composition ............................................................. 74
4.3.3 Estuarine food chains identified by Hg and N isotopes ............................................ 77
4.4 Discussion ........................................................................................................................ 78
4.4.1 Hg isotope ratios distinguish dominant MeHg sources for fish ................................ 78
4.4.2 Hg isotopes indicate life history ................................................................................ 79
4.4.3 Environmental sources of inorganic Hg and MeHg in Labrador Sea ....................... 81
4.4.4 Environmental processes of MeHg in freshwater tributaries and Lake Melville ...... 85
Supplemental Materials ................................................................................................................ 88
Chapter 5. Conclusions and future studies .................................................................................... 95
5.1 Key findings .................................................................................................................... 95
5.2 Future work ...................................................................................................................... 97

v
List of Figures
Figure 2.1. δ202Hg (‰) and Δ199Hg (‰) values in human hair (triangles) and seafood (x’s) from
the Faroe Islands and Gulf of Mexico regions. ..................................................................... 15!
Figure 2.2. Fraction of total MeHg exposure due to consumption of oceanic fish for Gulf of
Mexico anglers. ..................................................................................................................... 19!
Figure 2.3. Values of Δ199Hg (‰) for pilot whales (blue arrow) from this study and nine species
of marine fish (yellow circles) that feed at different depths in the central North Pacific
Ocean (Blum et al., 2013). Also shown is the depth preference for the main prey item of
pilot whales (squid, Todarodes sagittatus). ........................................................................... 21!
Figure 3.1. Distribution of high-frequency fish consumers across the U.S. relative to the Census
population in 2010. ............................................................................................................... 39!
Figure 3.2. Distributions of hair Hg concentrations: (a) measured concentrations; (b) modeled
concentrations corresponding to self-reported exposures. .................................................... 46!
Figure 3.3. Individual-level comparisons of paired modeled and measured hair Hg concentrations
in high-frequency consumers (n = 304). ............................................................................... 47!
Figure 3.4. Stable Hg isotope ratios measured in hair samples and consumed seafood types. .... 50!
Figure 4.1. Isotopic composition of subarctic fish from the Lake Melville, Labrador region. ..... 76!
Figure 4.2. Differences in stable isotope ratios between juvenile and adult smelt. p-values signify
the difference of mean response variable between juvenile and adult from t-test. ............... 81!
Figure 4.3. Compiled Hg isotopic data of fish from this study (LM), Gulf of Mexico (GoM)
(Senn et al., 2010), north Pacific Ocean (N. Pacific) (Blum et al., 2013), and north Atlantic
Ocean (N. Atlantic). .............................................................................................................. 83!
Figure S4.1. Map of the fish harvesting locations (yellow stars) for species included in this study.
Lake Melville is an estuarine fjord in Labrador, Canada. ..................................................... 90!
Figure S4.2. Mean δ13C of different fish species (error bar signifies standard deviation, color
shades represent the δ13C ranges of particulate organic matters in Lake Melville system:
river-Goose bay (green); central lake (purple); Goswater bay-Labrador Sea (blue). ........... 91!
Figure S4.3. Boxplots of fish isotopic compositions by their ecological zones: (a) Δ199Hg; (b)
δ202Hg; (c) δ13C. .................................................................................................................... 92!
Figure S4.4. (a) Hg stable isotope ratios of flatfish. Lower panel displays the trend of (b) Mass-
independent fractionation signature Δ199Hg; (c) Mass-dependent fractionation signature
δ202Hg; (d) δ15N; (e) δ13C along growth. ............................................................................. 93!
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Figure S4.5. Estimated range of mixed MeHg sources (dashed lines) from both freshwater and
marine environments by convex hull TA method (Layman et al., 2007). ............................ 94!

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List of Tables
Table S2.1. Mercury concentrations and isotope ratios in standards and samples (a: Faroese
whalers and pilot whales; b: GOM anglers). ........................................................................ 29!
Table S2.2. Comparison of estimated fractions of MeHg from oceanic fish based on dietary
recall (frecall) and the isotope mixing model based on Δ199Hg and δ202Hg (f and
hair hair MIF
f ). The ranges of f and f based on the sensitivity analysis with variable fish Hg
MDF MIF MDF
isotope ratios (±SD) are shown in parenthses. ...................................................................... 32!
Table S2.3. Percentages of total MeHg exposure from each fish species accounting for most of
the MeHg exposure for each individual based on the dietary survey. Fish species with
percentages <5% were not included. .................................................................................... 33!
Table 3.1. Methylmercury concentrations (µg g-1) in different seafood types used to derive intake
based exposure estimates. ..................................................................................................... 55!
Table 3.2. Pharmacokinetic parameters used in one-compartment model to calculate hair Hg
equivalents corresponding to self-reported MeHg intake. .................................................... 56!
Table 3.3. Multivariate linear regression of the natural log of measured hair Hg levels (µg g-1). 57!
Table S3.1. Contributions to MeHg exposure from different seafood types in hair samples
analyzed for Hg isotopes (see Figure 4, main text). ............................................................. 61!
Table S3.2. Demographic data corresponding to hair samples analyzed for Hg isotopes. ........... 62!
Table S3.3. Stable Hg isotope data for high-discrepancy (ID 1-8) and low-discrepancy (ID 9-16)
samples. ................................................................................................................................. 63!
Table S3.4. Linear regression of the natural log of discrepancy between modeled and measured
hair Hg levels (R square =0.29). ........................................................................................... 64!
Table 4.1. Hypothesized predominant MeHg production source taken up by fish species based
on literature data on prey and primary habitat. ..................................................................... 74!
Table S4.1. Habitat and prey preferences of all fish species from Lake Melville fjord. .............. 88!
Table S4.2. Descriptive statistics (mean±standard deviation) of length, age, Hg concentrations,
MeHg fractions, and δ15N of each species. .......................................................................... 89!

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Acknowledgments
First and foremost I want to thank my advisor—Elsie Sunderland who has been
tremendously helpful throughout my doctoral research. Her guidance has a vital significance in
shaping me as a scientist and as a future mentor. Elsie is very respectful to my ideas and I really
enjoy the numerous hours we spent together for discussing and improving my work as well as
generating new research ideas. I have my most genuine gratitude to her for keeping me always
curious about science and leading me to be an independent researcher. I am also grateful to have
James Shine as my co-advisor in past five years. Jim’s enthusiastism for science has created
many opportunites for me to work, including my very first Hg isotope project which brought me
into this exciting and fast-growing field.
Second, I would like to acknowledge my collaborators and co-authors. Especially, for my
first chapter, Laura Sherman and Joel Blum generously shared their expertise on Hg isotope with
me, which was extremely helpful for me to quickly become newcomer in this field. Additionally,
Laura has dedicated much time and effort to discussing data and improving my writing for
publication. I also want to thank Philippe Grandjean, Bjarni Mikkelsen, and Pál Weihe for
providing samples and insights for my chapter. For the second chapter, I would like to thank
Katherine von Stackelberg and Christoph Rheinberger, and James Hammitt for their advice on
my data analysis of fish consumption data and writing improvement which made this chapter’s
major scientific contribution much clearer. For both second and third chapters, Runsheng Yin
and David Krabbenhoft have been very supportive for my Hg isotope analysis and I want to
thank their various intellectual input and their hospitality for hosting me to do analysis in their
lab. Thank Amina Schartup, Amelia Valberg and Jessica Eward for doing so much work with me
on processing and analyzing fish samples as well as conducting thoughtful discussion. It has
been very fun and inspiring to work with all of my collaborators.
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Thank you also to my fellow graduate students and postdocs. I would especially like to
thank the aquatic biogeochemistry group members from both SEAS and SPH including Helen
Amos, Amina Schartup, Dan Madigan, Xianming Zhang, Yanxu Zhang, Hannah Horowitz, Ryan
Calder, Clifton Dassuncao, Xindi Hu, Anne Soerensen, Asif Queshi, Sarah Jane White, Zhao
Dong, Yongmei Shen and Eun Joo Park. Their critical feedback and spiritual support helped me
go through the hard time and made many long hours in the lab and office enjoyable. I also want
to thank the lab managers Nick Lupoli (at SPH) and Prentiss Balcom (at SEAS) for all their time
on training and assisting me to do various chemical analyses. I also appreciate the advice from
experts in Hg isotope field outside Harvard, especially Jeroen Sonke, Sae Yun Kwon, and Ryan
Lepak.
Finally, I would like to thank my family and friends within and outside of the Harvard
University. Thank you to my friends Yili Pan, Chong Zhang, Joshua Cregger, Eun Joo Park,
Yongmei Shen, Emily Sparer, Wan-Chen Lee, Souzana Achilleos, Sophia Qiu and many others.
My life is sunnier with your company. Thank you to my parents for always encouraging me to
pursue whatever I truly like. To be their child is the most fortunate thing in my life and I believe
the optimism and persistence inherited from them are the two major features helping me to
achieve this accomplishment. Thank you to Jessie & Bill Shun for their support and care
throughout my U.S. life. I wish uncle Bill could be here to share this accomplishment.

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