Biogeochemical analysis of ancient Pacific Cod bone suggests Hg bioaccumulation was linked to paleo sea level rise and climate change

Deglaciation at the end of the Pleistocene initiated major changes in ocean circulation and distribution. Within a brief geological time, large areas of land were inundated by sea-level rise and today global sea level is 120 m above its minimum stand during the last glacial maximum. This was the era of modern sea shelf formation; climate change caused coastal plain flooding and created broad continental shelves with innumerable consequences to marine and terrestrial ecosystems and human populations. In Alaska, the Bering Sea nearly doubled in size and stretches of coastline to the south were flooded, with regional variability in the timing and extent of submergence. Here we suggest how past climate change and coastal flooding are linked to mercury bioaccumulation that could have had profound impacts on past human populations and that, under conditions of continued climate warming, may have future impacts. Biogeochemical analysis of total mercury (tHg) and δ 13C/δ15N ratios in the bone collagen of archeologically recovered Pacific Cod (Gadus macrocephalus) bone shows high levels of tHg during early/mid-Holocene. This pattern cannot be linked to anthropogenic activity or to food web trophic changes, but may result from natural phenomena such as increases in productivity, carbon supply and coastal flooding driven by glacial melting and sea-level rise. The coastal flooding could have led to increased methylation of Hg in newly submerged terrestrial land and vegetation. Methylmercury is bioaccumulated through aquatic food webs with attendant consequences for the health of fish and their consumers, including people. This is the first study of tHg levels in a marine species from the Gulf of Alaska to provide a time series spanning nearly the entire Holocene and we propose that past coastal flooding resulting from climate change had the potential to input significant quantities of Hg into marine food webs and subsequently to human consumers.

Introduction

The Gulf of Alaska is bordered on the west by Kodiak Island and the Alaska Peninsula and on the southeast by the Alexander Archipelago. Natural and human systems have intersected here for over 7500 years, with interactions accessible through archeological, geological and biogeochemical methods (Jordan, 2001; Gehrels, 2010; Hu et al., 2010). Faunal remains from coastal archeological sites indicate that people were focused on procuring marine resources from the time of initial settlement in the region (Yesner, 1998). Many sites display long sequences of archaeofauna, including Pacific Cod (Gadus macrocephalus). Today a commercially valuable species, Pacific Cod are significant as a component of the ecosystem and because of their broad distribution on the shelf in the North Pacific (Beamish, 2008). Their skeletal remains, preserved in archeological deposits, offer, through biogeochemical analyses, the potential to reflect past ecosystem changes and a window into climate-related impacts on marine food webs.

Stable carbon and nitrogen isotope ratios (δ¹³C/δ¹⁵N) in the bone collagen and other hard tissues of marine species serve as proxies for primary productivity and food web interactions. The δ¹³C values are linked to primary productivity by fractionation due to the photosynthetic rate in phytoplankton (Laws et al., 1995) and differing ocean productivity regimes (Bidigare et al., 1997). Temporal changes in the δ¹³C in whale baleen from the Bering Sea and the bone collagen of pinnipeds from the North Pacific appear to track changes in marine productivity (Schell, 2000; Hirons et al., 2001), and the former possibly indicate changes in sea-ice cover (McRoy et al., 2004). Changes in the length of the food web are reflected in the δ¹⁵N values in tissues of marine vertebrates (Minagawa and Wada, 1984), including bone collagen. Periods of very high or low productivity may alter the length of food webs by increasing or decreasing available food, and may alter the trophic level of marine organisms as measured by δ¹⁵N (Fry and Sherr, 1984; Hobson and Welch, 1992). Depending upon the trophic position of a consumer within a marine food web, exposure to Hg varies (Selvaraj et al., 1997; Hsu et al., 2006). The comparison of Hg exposure risk over time and space is an important environmental health issue for both wildlife and people (Dehn et al., 2006). In humans there is a correlation between exposure to Hg and behavioral changes, including central nervous system deficit affecting fetal development and growth of young (Walker, 2014). Mercury is readily absorbed through the respiratory and gastrointestinal tracts; it bioaccumulates and is subject to biomagnification by trophic transport from lower to higher levels (Atwell et al., 1998; Dorea, 2008; Dunlap et al., 2011; Stern et al., 2012).

Besides being emitted from various locations in temperate latitudes and via industrial enterprise, Hg is naturally present in Alaskan and Siberian mountainous formations and sediments (Sunderland et al., 2009). Mercury ores occur in orogenic belts around relatively young mountains, hot springs or volcanic regions (Rytuba, 2003). Mercury has a crustal abundance of approximately 40–80 ppb but ore deposits can exceed 0.1% mercury. Mercury may become bioavailable in the marine environment through a number of natural processes including flooding leading to microorganism methylation of biologically bound inorganic Hg (Stokes and Wren, 1987) and water-column methylation of inorganic Hg in polar waters (Lehnherr et al., 2011).

Materials and Methods

Mercury concentrations can be determined in archeological specimens of bone, hair, fur, and teeth (Gerlach et al., 2006; Outridge et al., 2009). We sampled angular bones from individual ancient Pacific Cod recovered from archeological deposits at the XMK-030 site, located on a small island in Shelikof Strait, Gulf of Alaska (Figure 1), for Hg. Twenty of these bones were analyzed for both Hg and δ¹³C/δ¹⁵N. An additional 25 were analyzed for just Hg and additional 8 for just ratios of δ¹³C/δ¹⁵N. We also analyzed Hg concentrations in muscle tissue of 63 modern Pacific Cod from the same region.

FIGURE 1

Figure 1. Figure shows the extent of the shelf area formed after deglaciation and the location of the study area. XMK-030 is a small island located in the Shelikof Strait of the Gulf of Alaska. It was home to human inhabitants for nearly 7000 years. Archeological samples discussed here were recovered from XMK-030 by archeologists from the US National Park Service. Bathymetric map courtesy of NOAA Pacific Marine Envirnmental Laboratory, inset map showing the project area drafted by M. Hilton.

The archeologically recovered bones sampled were associated with radiometrically-dated strata in the XMK-030 deposits (Table 1). The lower section of the site which is a compact sediment matrix has many stratigraphically distinct human occupation floors, some attached to shell and bone middens, with an age range from 7600 to 4100 rcy BP. These deposits are overlain by a meter of sterile Aeolian sand, in turn, capped by a three-meter-thick loose shell and bone midden deposited between 2010 and 370 rcy BP.

TABLE 1

Table 1. Pacific Cod archeological bone samples: provenience, biogeochemical data and associated radiocarbon samples.

Stable Isotope Analysis

We measured ratios of δ¹³C/δ¹⁵N and Hg concentrations in an effort to identify change, if any, in marine production, food web and Hg accumulation, from the early Holocene to the present. Methods for δ¹³C/δ¹⁵N analysis and Hg analysis are also described elsewhere (Hirons, 2001; Rothschild and Duffy, 2005; Dunlap et al., 2011).

Bone samples were well preserved and free of humus and tissues, collagen was extracted following the procedure described in detail in Hirons (2001). Approximately 0.5 g of bone was sonicated and the lipids were removed with a methanol/chloroform procedure before being demineralized. The bone samples were allowed to demineralize in 1N HCl for approximately 4 days at 5°C; fresh acid was added to the samples every day. The remaining collagen matrix was then rinsed in deionized water until a neutral pH was reached. Each sample was heated in deionized water below boiling temperature to dissolve the collagen and precipitate the peptides. The solution was passed through a 0.45 μ filter and filtrate was dried in a lypholizer for 24 h, until the collagen had thoroughly dried.

Mass Spectrometry

Subsamples of each tissue (0.2–0.4 mg) were combusted and analyzed for stable isotope rations with a Thermo-Finnigan Delta Plus isotope ratio mass spectrometer. Replicability of standards and samples was ≤0.2⁰/₀₀ for both δ¹³C and δ¹⁵N. Stable isotope ratios were expressed in the following standard notation:

$8\text{X}(°{/}_{00})={\text{R}}_{\text{sample}}/{\text{R}}_{\text{standard}}-1)\times 1000$

Where X is ¹³C or ¹⁵ N and R_sampleis the ¹³C/¹²C or ¹⁵N/¹⁴N respectively. R_standard for ¹³C is Pee Dee Belemnite; for ¹⁵N it is atmospheric N₂(air).

All sample processing was conducted at the University of Alaska Fairbanks and the mass spectrometric analysis of the samples was done at the Alaska Stable Isotope Facility.

Mercury Analysis

Bones were washed with detergent free of Hg and trace metals, rinsed with r.o. water, dried in a drying oven. Samples were shipped to Frontier Geosciences, Inc. for Hg analysis. Samples were analyzed by standard Cold Vapor Atomic Fluorescence Spectroscopy after standard digestion in 70% nitric acid followed by dilution with 10% bromine chloride and reduction with tin chloride (Gerlach et al., 2006).

Muscle tissue dry weight was determined in samples which were collected, dried, and placed in 40 mL certified; pre-cleaned quartz glass sample vials. These were stored a −20°C until analysis. Samples were digested with 70% HNO₃/30% H₂SO₄ in the vial and heated until all soft tissue was dissolved. After cooling, the digests were diluted with 10% 0.2 N BrCl. Fort, aliquots of digests were reduced with SnCl₂, followed by Cold Vapor Automatic Fluorescence (CVAF) detection (Rothschild and Duffy, 2005). Calibration curves were constructed to assess the accuracy of tHg determination; certified dogfish tissue (DORM-2) form the National Research Council of Canada was analyzed. A check standard and a blank were run after every 10 samples.

Results

The results of the δ¹⁵N isotope analysis indicate that the archeologically recovered cod showed little to no change in trophic position over time. This position is consistent with data from modern cod which feed epibenthically and/or demersally (Hobson and Welch, 1992; Yang, 2004). By contrast, carbon isotopes signatures become heavier over time, a likely result of flooding of the shelf and a transfer from an oceanic productivity regime to a shelf system (Figure 2). The increase in δ¹³C of organic carbon may have resulted from an increase in phytoplankton growth rates (Laws et al., 1995) or a change from pelagic to a more benthic foraging regime as sea level changed throughout the Holocene (France, 1995). For example, in the Bering Sea the productivity of the shelf sea is 20–40 times higher than the adjacent oceanic basin waters (Springer et al., 1996). The shelf sea was entirely formed by sea level rise over the early Holocene and sea level in the study area continued rising until about 4000 years ago (Mann et al., 1998), leading to an increse in coastal margin productivity (Day et al., 2007).

FIGURE 2

Figure 2. δ¹³C/δ¹⁵N values for Pacific cod. Figure shows δ values plotted vs. time with little to no change in δ¹⁵N and a trend to heavier δ¹³C values from the early Holocene (7000 rcy BP) to the more recent (ca 0.578 rcy BP). Total number of samples = 28.

The δ¹³C records of planktonic and benthic foraminifera from southern Bering Sea sediment cores indicated a change in ocean temperature and salinity consistent with intermediate water formation resulting from deglaciation (Gorbarenko, 1996). Carbon enriched sediment, resulting from C₃ and possibly also C₄ plants growing in the steppe-tundra region of the emergent shelf during glaciation, were transported across the continental shelf and Bering Sea basin, and settled to the benthos throughout the Holocene, thereby further enriching the organic carbon of the shelf community. The extent of C₄ plant distribution in Beringia is unclear although there are several species present today, and there is debate as to whether they may have been more common prior to deglaciation (Wooller et al., 2007).

The results of the Hg analysis (Figure 3) show an unexpected trend from high concentrations in the early/mid Holocene (ca. 52–4600 rcy BP) to low concentrations of approximately current crustal levels after about 1000 ybp. By this time sea level has long since stabilized but this is still prior to modern global anthropogenic contamination (Outridge et al., 2009). According to Nechaev et al. (1994), northeastern Bering Sea sediments also have a heavy mineral composition predominantly from volcanic sources within the region.

FIGURE 3

Figure 3. Trend in tHg concentrations in bone of Pacific cod. There is a decline in mean tHg concentrations from pre 5000 rcy BP. Total number of specimens = 45 archaeological, 63 modern. Crust values and modern cod muscle values are included as baseline references for the archeological cod values, while acknowleging that values across tissue types and over time may not be directly correlated. Cod predating 1437 rcy BP exhibit Hg concentrations that are higher than the crust values (dashed line) for the study area (Boehm, 2001). Bars indicate ng/g for total mercury ranging from 700 to 40 ng/g.

Hg concentrations in the muscle of modern cod from the Shelikof Strait region show tissue values in the range of 0.25–0.5 ppm, in agreement with other studies (Burger and Gochfeld, 2007). While Pacific cod muscle tissue is not directly comparable to the cod bone, average Hg concentrations in the soft tissue of waterfowl may be up two times higher than in bone (Rothschild and Duffy, 2005) while other studies indicate that there is a correlation between hard tissue (teeth) and soft-tissue Hg concentrations in some mammals (Eide and Wesenberg, 1993; Outridge et al., 2000). The inclusion of the cod muscle Hg data here is intended to provide some comparative modern baseline for the archeological materials. No Hg values are available for modern cod bone and as of yet there are no comparative tissue studies for fish that include bone but, Hg mercury levels in Pacific cod are reported elsewhere in concentrations appropriate to the cod's trophic level (Burger and Gochfeld, 2007).

Discussion

We suggest that concentrations of Hg in Pacific Cod have fluctuated through the Holocene in concert with major paleoclimatic events, and more recently with increased anthropogenic inputs of Hg into the environment (Outridge et al., 2009). The main driver of Hg bioaccumulation in the early Holocene is proposed to be the methylation of Hg caused by the innundation of vegetation and soils across vast tracts of land at the end of the Pleistocene and through the early Holocene as a result of sea level rise due to deglaciation. A smaller-scale example of this process occurs when rivers are dammed to form hydroelectric reservoirs (Dmytriw et al., 1995). The large freshwater impoundments flood the land and lead to high levels of Hg in fish and other species (Brinkmann and Rasmussen, 2010). In this instance, we find high levels in an important subsistence species, Pacific Cod, suggesting a potential Hg exposure to prehistoric human populations not previously recognized.

Our data show Hg in the oldest cod bones occurs in concentrations approximating those in the flesh of modern cod. This is a previously unrecognized source of Hg to human consumers during the early Holocene. The concentrations in our samples fall to approximately the crustal level of Hg after about 1000 rcy BP (Figure 3). By this time sea level has long since stabilized to a still stand. This is still prior to modern global anthropogenic contamination (Outridge et al., 2009). These high concentrations early in the Holocene cannot be linked to any anthropogenic source of Hg. Elsewhere in the new world impacts from anthropogenic Hg associated with mining appear as early as 2400 years ago, but were localized until probably the fifteenth century (Cooke et al., 2011). Methlyation of biologically bound inorganic Hg and water-column methylation of inorganic Hg are the likely causes, driven in large part by sea level rise (Stokes and Wren, 1987; Boehm, 2001).

Mercury continues to be a health issue, and with industrial sources coupled with atmospheric transport and climate change, the potential to impact global food webs and the concomitant risk to human consumers in the coming decades are not insignificant. Based on variable projections of sea level rise under continued conditions of climate change (Grinsted et al., 2010) we suggest that Hg methylation from currently terrestrially bound sources should be factored into future projections of Hg bioavailability and impact to human and marine ecosystem health.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

This research was supported by NSF Award #0525275. Holly McKinney assisted with the selection of archeological Pacific Cod remains for analysis and assisted with some of the stable isotope sample preparation.

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