Grizzly Bear Hair Reveals Toxic Exposure to Mercury through Salmon

Jun 5, 2014 - Stantec Consulting Ltd., 2042 Mills Road, Unit 11, Sidney, British Columbia V8L 4X2, Canada. ‡. School of Earth and Ocean Sciences, ...
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Grizzly Bear Hair Reveals Toxic Exposure to Mercury through Salmon Consumption Marie Noel̈ ,† Jody Spence,‡ Kate A. Harris,† Charles T. Robbins,§ Jennifer K. Fortin,∥ Peter S. Ross,⊥ and Jennie R. Christensen*,† †

Stantec Consulting Ltd., 2042 Mills Road, Unit 11, Sidney, British Columbia V8L 4X2, Canada School of Earth and Ocean Sciences, University of Victoria, Bob Wright Centre A405, P.O. BOX 3065 STN CSC, Victoria, British Columbia V8W 3V6, Canada § School of the Environment and School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236, United States ∥ USGS Alaska Science Center, 4210 University Drive, Anchorage, Alaska 99508, United States ⊥ Ocean Pollution Science Program, Vancouver Aquarium, P.O. Box 3232, Vancouver, British Columbia V6B 3X8, Canada ‡

S Supporting Information *

ABSTRACT: Mercury obtained from the diet accumulates in mammalian hair as it grows thus preserving a record of mercury intake over the growth period of a given hair segment. We adapted a microanalysis approach, using laser ablation inductively coupled plasma mass spectrometry, to characterize temporal changes in mercury exposure and uptake in wild and captive grizzly bears. Captive grizzlies fed diets containing known and varied amounts of mercury provided data to allow prediction of Hg ingestion rates in wild bears. Here, we show, for the first time, that 70% of the coastal grizzly bears sampled had Hg levels exceeding the neurochemical effect level proposed for polar bears. In a context where the international community is taking global actions to reduce Hg emissions through the “Minamata Convention on Mercury”, our study provides valuable information on the exposure to mercury of these grizzly bears already under many threats.



INTRODUCTION Mercury (Hg) remains a contaminant of concern for the health of the environment. It bioaccumulates up the food chain in its methylated form and can cause a variety of short and long-term toxic effects in top predators such as grizzly bears (Ursus arctos horribilis). Globally, mercury is emitted from both natural (∼60% of the total atmospheric Hg emissions, most of which includes re-emissions from past deposition) and anthropogenic sources,1 among which fossil fuel fired power plants and artisanal small scale gold mining activities are dominant.2 In British Columbia (BC), there is a long history of local mercury contamination with the most significant contamination period (1965−1975) being associated with mercury discharge from a chlor-alkali plant at the head of Howe Sound.3 In addition, with prevailing winds from the west delivering air masses to North America from Asia in only 2−10 days,4,5 Asian emissions contribute between 15% and 24% of mercury deposition over the western United States.6,7 In an international effort to reduce mercury emissions and their impacts on the environment, the “Minamata Convention on Mercury” was formally adopted in October 2013. However, recent estimates still suggest future increase in global anthropogenic Hg emissions as a result of an © 2014 American Chemical Society

increase from the largest contributor, East Asia, which accounts for nearly 40% of the total.2 Taken together, this information suggests that mercury might be of concern for coastal ecosystems of western North America. The grizzly bear is a keystone species in northwestern North America, consuming a variety of foods including plants, berries, insects, mammals, and carrion. Individuals inhabiting coastal areas also rely heavily on Pacific salmon (Oncorhynchus spp.) in the fall,8,9 a trait which is linked to increased reproductive success and overall fitness of the population.10 However, salmon are also biovectors of Hg,11,12 a contaminant known for its deleterious effects on mammalian immune and neurological systems.13,14 Given the omnivorous and opportunistic nature of BC grizzly bears, mercury uptake over time may be expected to vary widely among individuals. The ability of hair to resist chemical changes makes it a unique biomatrix with which to assess mercury exposure in Received: Revised: Accepted: Published: 7560

February 6, 2014 June 5, 2014 June 5, 2014 June 5, 2014 dx.doi.org/10.1021/es500631g | Environ. Sci. Technol. 2014, 48, 7560−7567

Environmental Science & Technology

Article

Figure 1. Hair samples were collected from a total of 20 grizzly bears at various locations in coastal and interior British Columbia, Canada.

mammals.15 Unlike blood or other biological tissues that are used in eco-toxicological studies which have transient pharmacokinetic properties, hair is resistant to hydrolysis and/or enzyme activity and is considered to have a stable composition.16 Hair therefore preserves a record of mercury intake and, unlike most biological tissues, can be noninvasively sampled and requires no special storage or handling. As a result, whole hair analysis of trace metal elements has been widely used in human17−19 and various wildlife species including river otters (Lutra Canadensis),20 polar bears (Ursus maritimus),21 harbor seals (Phoca vitulina),22 and reindeer (Rangifer tarandus).23 While the majority of studies on trace metals in hair used atomic fluorescence spectrometry (AFS)23 or cold vapor atomic absorption spectrometry (CV-AAS),18,20 some studies have used more advanced, powerful techniques such as synchrotronX-ray fluorescence (SXRF)24−26or laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS)27−29 to allow

for high resolution analysis. Here, we use LA-ICP-MS to measure Hg variations along the entire length of individual grizzly bear hairs with high spatial resolution and provide millimeter scale data. This means that individual hair can provide information on Hg levels over short intervals, sometimes shorter than a day.27,28 Such high resolution analysis is not practical with most other methods as the resolution is set by physically cutting the hair into segments and separately processing and analyzing each individual piece. The sensitivity of LA-ICP-MS therefore allows for the noninvasive collection of detailed Hg data from a single hair, an important consideration when it comes to studying evasive or dangerous wildlife such as grizzly bears. In the present study, the first application of LA-ICP-MS to hair sampled from wildlife, we investigated temporal changes in mercury exposure and uptake in wild and captive grizzly bears. It provides the first information on mercury levels in BC grizzly 7561

dx.doi.org/10.1021/es500631g | Environ. Sci. Technol. 2014, 48, 7560−7567

Environmental Science & Technology

Article

Figure 2. Hg levels along the hair of the captive grizzly bears revealed strong Hg signals related to fish consumption. (a) Five captive grizzly bears were involved in a year-long feeding trial at the Washington State University Bear Research, Education, and Conservation Facility in Pullman, WA, USA. During a 33-day period (May 30−July 1 2006), bears were fed varying amounts of Yellowstone Lake cutthroat trout containing mercury concentrations at least 2 orders of magnitude higher than their standard feed.30 (b) Hair samples were collected along the middle of the bear back in late October just prior to hibernation. Sharp increases in Hg levels in the five bears coincided with the period of consumption of trout before decreasing after the end of the fish consumption period. (c) Linear increases in Hg concentrations in hair samples were observed throughout the trout consumption period. (d) There was a relationship between Hg accumulation rate in the hair and Hg intake through the diet (y = 0.114 × (1 − e−0.48x)); r2 = 0.99; p < 0.001). (e) Shortly after the end of the fish consumption period, Hg concentrations decreased exponentially with time. (f) Half-lives appeared to decrease with increasing Hg intake at low Hg levels but seemed to level off around 0.5 μg/kg bear/day (r2 = 0.87; p = 0.038).

ratio. In addition, samples from five captive grizzly bears involved in a year-long feeding trial30 were collected at the Washington State University Bear Research, Education, and Conservation Facility, USA. Bears from this facility are described as healthy females having previously produced several sets of healthy cubs.31 Briefly, captive grizzly bears were fed, separately, various and known amounts of Yellowstone Lake cutthroat trout (Figure 2a) for a 33-day period (May 30−July 1, 2006). Mercury levels in the trout were at least 2 orders of magnitude higher (∼0.5 μg/g) than those reported in the standard captive bear diet (