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Carbon, nitrogen and mercury isotope evidence for the biogeochemical history of mercury in Hawaiian marine bottomfish Dana Sackett, Jeffrey C Drazen, Brian N. Popp, C. Anela Choy, Joel D. Blum, and Marcus W. Johnson Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b04893 • Publication Date (Web): 14 Nov 2017 Downloaded from http://pubs.acs.org on November 15, 2017
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Environmental Science & Technology
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Title: Carbon, nitrogen and mercury isotope evidence for the biogeochemical history of mercury
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in Hawaiian marine bottomfish
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Authors: Dana K. Sackett*1, Jeffrey C. Drazen2, Brian N. Popp3, C. Anela Choy4, Joel D. Blum5,
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Marcus W. Johnson5
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Addresses: 1School of Fisheries, Aquaculture, and Aquatic Sciences, Auburn University,
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Auburn, AL 36849, USA; 2Department of Oceanography, University of Hawaii, Manoa, 1000
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Pope Road, Honolulu, HI 96822, USA; 3Department of Geology and Geophysics, University of
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Hawaii, Manoa, 1680 East-West Road, Honolulu, HI, 96822, USA; 4Monterey Bay Aquarium
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Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA; 5Department of Earth
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and Environmental Sciences, University of Michigan, 1100 N University Avenue, Ann Arbor,
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Michigan 48109, USA.
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*Corresponding author: 1School of Fisheries, Aquaculture, and Aquatic Sciences, Auburn
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University, Auburn, AL 36849, USA; phone: 910-578-1088;
[email protected] 17 18 19 20 21 22 23
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Abstract - The complex biogeochemical cycle of Hg makes identifying primary sources of fish
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tissue Hg problematic. To identify sources and provide insight into this cycle, we combined
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carbon (δ13C), nitrogen amino acid (δ15NPhe), and Hg isotope (∆199Hg, ∆201Hg, δ202Hg) data for
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six species of Hawaiian marine bottomfish. Results from these isotopic systems identified
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individuals within species that likely fed from separate food webs. Terrestrial freshwater inputs
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to coastal sediments were identified as the primary source of tissue Hg in the jack species,
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Caranx ignobilis, which inhabit shallow marine ecosystems. Thus, coastal C. ignobilis were a
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biological vector transporting Hg from freshwater environments into marine ecosystems. Depth
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profiles of Hg isotopic compositions for bottomfish (excludung C. ignobilis) were similar, but
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not identical, to profiles for open-ocean pelagic fishes, suggesting that in both settings inorganic
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Hg, which was ultimately transformed to monomethylmercury (MeHg) and bioaccumulated, was
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dominantly from a single source. However, differences between pelagic fish and bottomfish
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profiles were attributable to mass-dependent fractionation in the benthos prior to incorporation
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into the food web. Results also confirmed that bottomfish relied, at least in part, on a benthic
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food web and identified the incorporation of deeper water oceanic MeHg sources into deeper
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water sediments prior to food web uptake and transfer.
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TOC:
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Environmental Science & Technology
Introduction Mercury (Hg) is a highly toxic global contaminant for which both humans and wildlife
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are primarily exposed through the consumption of fish (Hall et al. 1997; Mergler et al. 2007;
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Scheuhammer et al. 2007; Sunderland et al. 2009). Understanding the chemical and ecological
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pathways that lead to high Hg concentrations in fish tissue is, therefore, vital to managing human
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and wildlife health. While all forms of Hg are toxic, it is the organic monomethylmercury form
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(MeHg) that bioaccumulates in aquatic food webs (Bloom 1992; Hall et al. 1997; Harris et al.
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2003) and is most readily transferred to humans. MeHg is formed when bacteria methylate
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inorganic Hg, subsequent to deposition in terrestrial and aquatic environments (Gilmour et al.
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1992; DiGiulio et al. 2008). The environmental conditions (e.g., pH, oxygen, dissolved organic
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matter) where Hg is deposited influence Hg transport and net rates of Hg methylation (Ullrich et
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al. 2001; Ravichandran 2004; Lamborg et al. 2014). For example, lower oxygen and lower pH
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environments have been noted to support higher net Hg methylation rates resulting in higher fish
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tissue Hg concentrations (Sackett et al. 2009). There are also both abiotic and biotic pathways
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that lead to reduction of MeHg and inorganic Hg(II) to the more volatile elemental Hg (Hg0),
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allowing it to re-enter the atmospheric Hg pool (Amyot et al. 1997; Bergquist and Blum 2007;
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Blum et al. 2013). As such, the complex biogeochemical and ecological processes that dictate
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Hg concentrations in fish tissue (e.g., deposition, methylation, microbial and photochemical
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reduction, adsorption, transport, bioaccumulation, trophic interactions) make it difficult to
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determine the locations where and the conditions under which the Hg that resides in fish tissue
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was originally transformed into the more toxic and bioavailable MeHg form.
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Identifying sources of MeHg in fish tissue is critical to understanding the consequences that environmental changes have on the biogeochemical cycle of Hg and what those changes
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mean for human health policy and fisheries management (Lamborg et al. 2014). Previous studies
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have linked pelagic fish tissue Hg with sources of Hg using Hg isotope techniques (Gehrke et al.
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2011; Senn et al. 2010; Blum et al. 2013). Therefore, this relatively new technique could help
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provide more detailed information on the sources of MeHg in bottomfish. Unlike pelagic
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species, bottomfish are associated with benthic sediment, an additional potential source of
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MeHg. Shallow benthic populations are often found near a landmass and thus, freshwater and
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estuarine outflows are also potential sources of MeHg (Sackett et al. 2015). Thus, investigation
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of bottomfishes that reside and feed at distinctly different depths could help distinguish between
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these different sources of tissue Hg. Bottomfish selected for this study, four lutjanid (snapper)
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and two carangid (jack) species, are all economically important species, frequently consumed by
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residents of Hawaii and elsewhere (Haight et al. 1993; Sato et al. 2006; Mergler et al. 2007; FAO
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2010). These fish are all large predators with average trophic positions that range from 3.6 to
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4.5, and whose diets include benthic crustaceans, cephalopods, pelagic tunicates and fishes. Each
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species is associated with a distinctly different mean depth of occurrence (range: 80 to 250m),
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though individual specimens have been found from 0.5 ‰) MIF (Blum et al. 2014), ∆199Hg/∆201Hg ratios from natural tissue
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samples within this range of values are indicative of these photochemical processes acting on Hg
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prior to its incorporation into the food web. Indeed, numerous studies of fish from a variety of
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marine and estuarine ecosystems have supported these findings, reporting a very narrow range of
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∆199Hg/∆201Hg ratios between 1.2 and 1.36 (Figure 1A; Bergquist and Blum 2007; Gantner et al.
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2009; Senn et al. 2010; Gehrke et al. 2011; Li et al. 2016). More specifically, values closer to
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1.2 are indicative of marine environments, while values closer to 1.36 are often seen in
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freshwater systems (Blum et al. 2013). Thus, the very strong relationship between ∆199Hg and
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∆201Hg (R2=0.99; Figure 1A) and the similar ∆199Hg/∆201Hg for these bottomfish compared to
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marine pelagic fish results presented in Blum et al. (2013; Figure 1A), demonstrates that marine
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MeHg photodegradation was the primary driver of MIF.
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Microbial versus photochemical processes
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Tissue ∆199Hg and δ202Hg values for all species except C. ignobilis declined with depth in
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a manner similar to pelagic species from the NPSG (Figure 2). Thus, MeHg in bottomfish and
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pelagic species tissues underwent similar photochemical and biotic fractionation processes prior
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to incorporation into the food web. For instance, Hg in shallower bottomfish species underwent
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more MIF as a result of photodegradation in surface waters, whereas Hg in deeper water
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bottomfish included contributions from a deepwater source of Hg that underwent pelagic
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microbial degradation prior to incorporation into the food web (Blum et al. 2013; Sackett et al.
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2015). For pelagic species, these results indicated the primary source of inorganic Hg was
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atmospheric deposition to the surface of the ocean (Blum et al. 2013), which also indicates a
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similar inorganic source of Hg to all investigated bottomfish except C. ignobilis.
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The range in bottomfish tissue ∆199Hg values (0.86‰ to 2.96‰) and δ202Hg values (-
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0.87‰ to 1.23‰) along with the ∆199Hg/ δ202Hg ratio for all bottomfish analyzed in this study
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(0.96) showed that both photodegradation and microbial demethylation were important processes
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impacting the MeHg in bottomfish tissue (Figure 1A, B; Blum et al. 2013). A ∆199Hg/ δ202Hg
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value close to the experimentally determined (Bergquist and Blum 2007) ratio of 2.43 would
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indicate photochemical degradation as the dominant transformation process, whereas a value
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closer to 0 would signify microbial transformations as the dominant process (Blum et al. 2013).
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A value close to the experimental value was measured for samples of pelagic species from the
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North Pacific Subtropical Gyre (NPSG; Blum et al. 2013; Figure 1B), where partial
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photodegradation dominated transformation of MeHg prior to incorporation into the food web.
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However, a minor component of tissue Hg in these pelagic fish was attributable to a deepwater
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source of MeHg that had been partially demethylated by microbial action prior to incorporation
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into deeper water food webs (Blum et al. 2013). Here, the range in ∆199Hg values for bottomfish
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was much lower, while the range in δ202Hg values was higher than that of pelagic species from
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the NPSG (Blum et al. 2013), resulting in a much lower ratio of ∆199Hg/ δ202Hg (slope = 0.96;
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Figure 1B). Because photochemistry will affect ∆199Hg and δ202Hg, whereas bacterial
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demethylation will only affect δ202Hg values, the higher variability in δ202Hg values for Hawaiian
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bottomfishes showed that tissue Hg in these more benthic species underwent more microbial
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MDF prior to incorporation into the food web than did tissue Hg associated with pelagic species
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(Blum et al. 2013; Bergquist and Blum 2009; Sackett et al. 2015). Specifically, assuming that a
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slope of 2.43 for ∆199Hg/δ202Hg represents 100% MIF and a slope of 0 represents 100%
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microbial MDF (Bergquist and Blum 2007), a slope of 0.96 demonstrates that microbial
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degradation accounted for approximately 60% of Hg degradation prior to incorporation into the
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food web. Indeed, even when C. ignobilis, the shallowest species with the most benthic/coastal
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δ13C values, is excluded, this ratio is 1.24 (P0.05). These results confirm, as others have
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(Senn et al. 2010, Bergquist and Blum 2007, Kritee et al. 2009, Gehrke et al. 2011), that when
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Hg is incorporated into a food web, MIF signatures are preserved and there is not additional
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fractionation with trophic transfers from prey to predator. However, overall bottomfish trophic
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position did increase significantly with mean depth of occurrence (Figure 4A). Overall, δ13C
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values also decreased with depth (Table 1; Figure 4B). Further, when the bottomfish species
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with the most pelagic dietary δ13C values were excluded (P. filamentosus; Sackett et al. 2015),
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the relationship between δ13C values and depth strengthened (P
