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Environmental Processes
Mercury stable isotopes reveal influence of foraging depth on mercury concentrations and growth in Pacific bluefin tuna Daniel James Madigan, Miling Li, Runsheng Yin, Hannes Baumann, Owyn E Snodgrass, Heidi Dewar, David P. Krabbenhoft, Zofia Baumann, Nicholas S. Fisher, Prentiss H. Balcom, and Elsie M. Sunderland Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b06429 • Publication Date (Web): 15 May 2018 Downloaded from http://pubs.acs.org on May 15, 2018
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Mercury stable isotopes reveal influence of foraging depth on mercury concentrations and growth in Pacific bluefin tuna Daniel J. Madigan*,1,†‡, Miling Li1,†, Yin Runsheng2,3, Hannes Baumann4, Owyn E. Snodgrass5, Heidi Dewar6, David P. Krabbenhoft3, Zofia Baumann4, Nicholas S. Fisher7, Prentiss Balcom1, Elsie M. Sunderland1,8
Affiliations: 1
Harvard John A. Paulson School of Engineering and Applied Science, Cambridge, MA USA
2
State Key Laboratory of Ore Deposit Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang 550002, China
3
U.S. Geological Survey, Middleton, WI USA Department of Marine Sciences, University of Connecticut, Groton, CT USA 5 Ocean Associates, Southwest Fisheries Science Center, NMFS, NOAA, La Jolla, California 92037, United States 6 Fisheries Resources Division, Southwest Fisheries Science Center, National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA), La Jolla, California 92037, United States 7 School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY USA 8 Department of Environmental Health, Harvard T. H. Chan School of Public Health, Boston, MA USA 4
†
These authors contributed equally to this work
‡
Now at: Gulf of California International Research Center, Santa Rosalía, BCS, Mexico
*
[email protected] +1 (516) 680-6470
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ABSTRACT
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Pelagic ecosystems are changing due to environmental and anthropogenic forces, with uncertain
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consequences for the ocean’s top predators. Epipelagic and mesopelagic prey resources differ in
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quality and quantity, but their relative contribution to predator diets has been difficult to track.
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We measured mercury (Hg) stable isotopes in young (1 year residency in the EPO to recent migration
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from the WPO29, 30, 32. Thus, PBFT were selected from a narrow size range, and focused on small
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individuals (66.3 to 76.0 cm FL) to minimize differences in migratory histories. Selection of
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these small fish, combined with information of migratory histories from otolith
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microchemistry35, allowed for some minimization of the confounding factor of varying migratory
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histories, especially use of the EPO versus the WPO.
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PBFT ages based on sagittal otolith analysis ranged from 328 – 498 days35, with an
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estimated coefficient of variation of 5.7%. Individual PBFT weight could not be directly and
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accurately determined from samples provided by fishermen due to variable treatment of fish
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(blood removed, viscera removed, etc). Muscle samples (~20 g) were obtained from the dorsal
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musculature ~2 cm below the skin. PBFT prey (Table S1) were collected directly in the field or
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from predator stomach contents. All prey were identified to genus or species using
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morphological characters. Prey from the WPO were collected from surface neuston tows, deep
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Ocean Research Institute (ORIs), and Isaacs-Kidd Midwater Trawls (IKMTs) during two
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research cruises in May and September 2013. Prey from the EPO were obtained both by trawl
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net in July 2015 off central CA, USA and from stomach contents33. Muscle tissue was collected
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from the dorsal musculature below the skin (fish), from the mantle (cephalopods), or from within
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the carapace (crustaceans).
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Hg concentration, prey energy density, and prey categorization.
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All samples were freeze-dried and homogenized using a Wig-L-Bug tissue grinder prior
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to any chemical analysis. The total Hg (THg) content of all PBFT and prey white muscle tissue
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was measured using a Nippon MA-3000 direct thermal decomposition Hg analyzer. The average
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recovery of the certified reference material (DORM-4) was 98.3 ± 6.1% SD (n = 4). Standard
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solution and DORM-4 calibration checks were performed every ten samples to monitor stability
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of the instrument. Samples were run in duplicate for every 10 samples, and overall variation of
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duplicates was < 3%. Hg concentrations are reported in µg g-1 dw, and means as mean (µg g-1
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dw) ± SD.
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All samples with adequate mass were analyzed for MeHg. Lyophilized and powdered
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samples were digested in 5N HNO3 at 60°C overnight and neutralized with 8 M KOH. MeHg
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was measured using a Tekran 2700 Automated MeHg Analysis System following EPA 1630
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method36. Recoveries of certified reference material DORM-4 (fish muscle) and TORT-3
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(lobster hepatopancreas) were 86.4 ± 6.3% SD (n = 8). Variability among sample duplicates was
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10.7 ± 4.8% (n = 9). For prey samples with inadequate tissue mass for MeHg analyses,
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concentrations were estimated by using species-specific mean MeHg as a fraction of total Hg
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(%) from the same species.
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Mean energy density values (kJ g-1 ww) were obtained for each prey species analyzed for
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Hg from a literature survey of species-specific values (Figure 1; Table S2). When available,
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species- and basin-specific energy densities were chosen. For cephalopods, a mean energy
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density from nine pelagic cephalopods in the EPO was used37. When unavailable for WPO fish
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species, energy density of that species in the EPO was used. We also obtained peak abundance
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and depth ranges for each species from the literature (Table S2).
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Hg isotope analysis. Approximately 0.1 – 0.2 g of ground sample was digested (120°C, 6 hours) in a 4 mL
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acid mixture (HCl:HNO3 = 1:3, v:v) for Hg isotope analysis, following previous studies25, 38, 39.
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Four types of certified reference materials (TORT-2, TORT-3, DORM-2, DORM-4) and blanks
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(n=5) were prepared in the same way as tissue samples. Based on measured total Hg
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concentrations, the digest solutions were diluted to 0.3 – 1.0 ng mL-1, depending on the
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availability of sample mass. A Neptune Plus multicollector inductively coupled plasma mass
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spectrometer (MC-ICP-MS) housed at Wisconsin State Laboratory of Hygiene was used to
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measure Hg isotopes. Details of instrumentation setup, operation conditions, and analytical
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methods are described in Yin et al.40 and Li et al.25. Total Hg in the diluted solutions was also
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monitored by MC-ICP-MS using 202Hg signals, which yielded mean recoveries of 93±9.2% and
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92±11% for fish samples (n=75) and certified reference materials (CRMs; n=10), respectively.
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The sensitivity for 202Hg during Hg isotope analysis is estimated to be 1.0 – 1.2 V per ng mL-1
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Hg. The signals for 202Hg were 103) and the ratio between ‘best draw’
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posterior and total posterior density (
