Concentrations of the genotoxic metals, chromium and nickel, in whales, tar balls, oil slicks, and released oil from the gulf of Mexico in the immediate aftermath of the deepwater horizon oil crisis: is genotoxic metal exposure part of the deepwater horizon legacy?

Concern regarding the Deepwater Horizon oil crisis has largely focused on oil and dispersants while the threat of genotoxic metals in the oil has gone largely overlooked. Genotoxic metals, such as chromium and nickel, damage DNA and bioaccumulate in organisms, resulting in persistent exposures. We found chromium and nickel concentrations ranged from 0.24 to 8.46 ppm in crude oil from the riser, oil from slicks on surface waters and tar balls from Gulf of Mexico beaches. We found nickel concentrations ranged from 1.7 to 94.6 ppm wet weight with a mean of 15.9 ± 3.5 ppm and chromium concentrations ranged from 2.0 to 73.6 ppm wet weight with a mean of 12.8 ± 2.6 ppm in tissue collected from Gulf of Mexico whales in the wake of the crisis. Mean tissue concentrations were significantly higher than those found in whales collected around the world prior to the spill. Given the capacity of these metals to damage DNA, their presence in the oil, and their elevated concentrations in whales, we suggest that metal exposure is an important understudied concern for the Deepwater Horizon oil disaster.

Metal Levels in Whales from the Gulf of Maine: A One Environmental Health approach.

One Environmental Health has emerged as an important area of research that considers the interconnectedness of human, animal and ecosystem health with a focus on toxicology. The great whales in the Gulf of Maine are important species for ecosystem health, for the economies of the Eastern seaboard of the United States, and as sentinels for human health. The Gulf of Maine is an area with heavy coastal development, industry, and marine traffic, all of which contribute chronic exposures to environmental chemicals that can bioaccumulate in tissues and may gradually diminish an individual whale's or a population's fitness. We biopsied whales for three seasons (2010-2012) and measured the levels of 25 metals and selenium in skin biopsies collected from three species: humpback whales (Megaptera novaeangliae), fin whales (Balaenoptera physalus), and a minke whale (Balaenoptera acutorostrata). We established baseline levels for humpback and fin whales. Comparisons with similar species from other regions indicate humpback whales have elevated levels of aluminum, chromium, iron, magnesium, nickel and zinc. Contextualizing the data with a One Environmental Health approach finds these levels to be of potential concern for whale health. While much remains to understand what threats these metal levels may pose to the fitness and survival of these whale populations, these data serve as a useful and pertinent start to understanding the threat of pollution.

A three year study of metal levels in skin biopsies of whales in the Gulf of Mexico after the Deepwater Horizon oil crisis.

In response to the explosion of the Deepwater Horizon and the massive release of oil that followed, we conducted three annual research voyages to investigate how the oil spill would impact the marine offshore environment. Most investigations into the ecological and toxicological impacts of the Deepwater Horizon Oil crisis have mainly focused on the fate of the oil and dispersants, but few have considered the release of metals into the environment. From studies of previous oil spills, other marine oil industries, and analyses of oil compositions, it is evident that metals are frequently encountered. Several metals have been reported in the MC252 oil from the Deepwater Horizon oil spill, including the nonessential metals aluminum, arsenic, chromium, nickel, and lead; genotoxic metals, such as these are able to damage DNA and can bioaccumulate in organisms resulting in persistent exposure. In the Gulf of Mexico, whales are the apex species; hence we collected skin biopsies from sperm whales (Physeter macrocephalus), short-finned pilot whales (Globicephala macrorhynchus), and Bryde's whales (Balaenoptera edeni). The results from our three-year study of monitoring metal levels in whale skin show (1) genotoxic metals at concentrations higher than global averages previously reported and (2) patterns for MC252-relevant metal concentrations decreasing with time from the oil spill.

Global assessment of cadmium concentrations in the skin of free-ranging sperm whales (Physeter macrocephalus).

Cadmium is a non-essential, toxic metal found accumulated in the organs of stranded cetaceans. Currently, there is no baseline cadmium concentration reported in a free-ranging, pelagic cetacean. The aim was to determine cadmium concentrations in the skin of free-ranging sperm whales (n=340) collected from 16 regions around the world during the voyage of the Odyssey (2000-2005) considering region, gender, and age in males. Cadmium was detected in 81% of skin biopsies with a mean of 0.3±0.04µg/g ww (0.02 to 12.4µg/g ww). These concentrations were higher than reported in literature in toothed whale skin (0.002-0.1µg/g ww). Concentrations by region were significantly different (p<0.0001) with the highest mean in Maldives and the Sea of Cortez (0.8 and 0.6µg/g ww, respectively). There was no significant difference in cadmium concentration by gender (p=0.42). Cadmium is known to have a long biological half-life, and cadmium concentrations in males were significantly higher in adults with a mean of 0.3µg/g ww compared to subadults with 0.2µg/g ww (p=0.03). Selenium, an element that binds to cadmium inhibiting its toxicity, had a moderately positive correlation with cadmium (r=0.41). Mercury, a toxic metal that positively correlates with cadmium in cetacean tissue, had a weakly positive relationship (r=0.20). The regional baselines reported in this study may be used to develop residue criteria for prediction of toxicological risk in sperm whale skin. Additionally, this study shows the extent of cadmium exposure in a pelagic cetacean that has global distribution.

Global assessment of oceanic lead pollution using sperm whales (Physeter macrocephalus) as an indicator species.

Lead (Pb) is an oceanic pollutant of global concern. Anthropogenic activities are increasing oceanic levels, but to an unknown extent. The sperm whale (Physeter macrocephalus) has a global distribution and high trophic level. The aim of this study was to establish a global baseline of oceanic Pb concentrations using free-ranging sperm whales as an indicator species. Skin biopsies (n=337) were collected during the voyage of the Odyssey (2000-2005) from 17 regions considering gender and age. Pb was detectable in 315 samples with a global mean of 1.6 ug/gww ranging from 0.1 to 129.6 ug/gww. Papua New Guinea, Bahamas and Australia had the highest regional mean with 6.1, 3.4, and 3.1 ug/gww, respectively. Pb concentrations were not significantly different between sex and age in males. This is the first global toxicological dataset for Pb in a marine mammal and confirms Pb is widely distributed with hotspots in some regions.

Global assessment of arsenic pollution using sperm whales (Physeter macrocephalus) as an emerging aquatic model organism.

Arsenic is an oceanic pollutant of global concern due to its toxicity, ability to bioaccumulate and continued input into the environment by anthropogenic activities. The sperm whale (Physeter macrocephalus) is an emerging aquatic model for both human disease and ocean health having global distribution and high trophic level. The aim of this study was to establish global and regional baselines of total arsenic concentrations using free-ranging sperm whales. Skin biopsies (n=342) were collected during the voyage of the Odyssey (2000-2005) from 17 regions considering gender and age in males. Arsenic was detectable in 99% of samples with a global mean of 1.9µg/g ww ranging from 0.1 to 15.6µg/g ww. Previous work in toothed whale skin found mean concentrations 3 fold lower with 0.6µg/g ww. A significant gender-related effect was found with males having higher mean arsenic concentrations than females. There was no significant age-related effect between adult and subadult males. Arsenic concentrations in sloughed skin samples were similar to levels in skin biopsies indicating that arsenic excretion can occur by skin sloughing. Regional mean concentrations were highest in the Maldives, Seychelles and Sri Lanka with 3.5, 2.5, and 2.4µg/g ww, respectively, raising concern for arsenic pollution in the Indian Ocean. Literature suggests that arsenic exposure is emitted from natural sources and the heavy use of arsenic-containing pesticides and herbicides in this region. These data suggest that research is needed in determining the extent and source of arsenic pollution in the Indian Ocean.

Global mercury and selenium concentrations in skin from free-ranging sperm whales (Physeter macrocephalus).

Pollution of the ocean by mercury (Hg) is a global concern. Hg persists, bioaccumulates and is toxic putting high trophic consumers at risk. The sperm whale (Physeter macrocephalus), is a sentinel of ocean health due to its wide distribution, longevity and high trophic level. Our aim was to survey Hg concentrations worldwide in the skin of free-ranging sperm whales considering region, gender and age. Samples were collected from 343 whales in 17 regions during the voyage of the research vessel, Odyssey, between 1999 and 2005. Skin was analyzed for total Hg and detected in all but three samples with a global mean of 2.5±0.1 µg g(-1) ranging from 0.1 to 16.0 µg g(-1). The Mediterranean Sea had the highest regional mean with 6.1 µg g(-1) followed by Australia with 3.5 µg g(-1). Considering gender, females and males did not have significantly different global Hg concentrations. The variation among regions for females was significantly different with highest levels in the Mediterranean and lowest in Sri Lanka; however, males were not significantly different among regions. Considering age in males, adults and subadults did not have significantly different Hg concentrations, and were not significantly different among regions. The toxic effects of these Hg concentrations are uncertain. Selenium (Se), an essential element, antagonizes Hg at equimolar amounts. We measured total Se concentrations and found detectable levels in all samples with a global mean of 33.1±1.1 µg g(-1) ranging from 2.5 to 179 µg g(-1). Se concentrations were found to be several fold higher than Hg concentrations with the average Se:Hg molar ratio being 59:1 and no correlation between the two elements. It is possible Hg is being detoxified in the skin by another mechanism. These data provide the first global analysis of Hg and Se concentrations in a free-ranging cetacean.

A global assessment of chromium pollution using sperm whales (Physeter macrocephalus) as an indicator species.

Chromium (Cr) is a well-known human carcinogen and a potential reproductive toxicant, but its contribution to ocean pollution is poorly understood. The aim of this study was to provide a global baseline for Cr as a marine pollutant using the sperm whale (Physeter macrocephalus) as an indicator species. Biopsies were collected from free-ranging whales around the globe during the voyage of the research vessel The Odyssey. Total Cr levels were measured in 361 sperm whales collected from 16 regions around the globe detectable levels ranged from 0.9 to 122.6 microg Cr g tissue(-1) with a global mean of 8.8+/-0.9 microg g(-1). Two whales had undetectable levels. The highest levels were found in sperm whales sampled in the waters near the Islands of Kiribati in the Pacific (mean=44.3+/-14.4) and the Seychelles in the Indian Ocean (mean=19.5+/-5.4 microg g(-1)). The lowest mean levels were found in whales near the Canary Islands (mean=3.7+/-0.8 microg g(-1)) and off of the coast of Sri Lanka (mean=3.3+/-0.4 microg g(-1)). The global mean Cr level in whale skin was 28-times higher than mean Cr skin levels in humans without occupational exposure. The whale levels were more similar to levels only observed previously in human lung tissue from workers who died of Cr-induced lung cancer. We conclude that Cr pollution in the marine environment is significant and that further study is urgently needed.