Roger Payne

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.

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.

What influences the worldwide genetic structure of sperm whales (Physeter macrocephalus)

The interplay of natural selection and genetic drift, influenced by geographic isolation, mating systems and population size, determines patterns of genetic diversity within species. The sperm whale provides an interesting example of a long‐lived species with few geographic barriers to dispersal. Worldwide mtDNA diversity is relatively low, but highly structured among geographic regions and social groups, attributed to female philopatry. However, it is unclear whether this female philopatry is due to geographic regions or social groups, or how this might vary on a worldwide scale. To answer these questions, we combined mtDNA information for 1091 previously published samples with 542 newly obtained DNA profiles (394‐bp mtDNA, sex, 13 microsatellites) including the previously unsampled Indian Ocean, and social group information for 541 individuals. We found low mtDNA diversity (π = 0.430%) reflecting an expansion event <80 000 years bp, but strong differentiation by ocean, among regions within some oceans, and among social groups. In comparison, microsatellite differentiation was low at all levels, presumably due to male‐mediated gene flow. A hierarchical amova showed that regions were important for explaining mtDNA variance in the Indian Ocean, but not Pacific, with social group sampling in the Atlantic too limited to include in analyses. Social groups were important in partitioning mtDNA and microsatellite variance within both oceans. Therefore, both geographic philopatry and social philopatry influence genetic structure in the sperm whale, but their relative importance differs by sex and ocean, reflecting breeding behaviour, geographic features and perhaps a more recent origin of sperm whales in the Pacific. By investigating the interplay of evolutionary forces operating at different temporal and geographic scales, we show that sperm whales are perhaps a unique example of a worldwide population expansion followed by rapid assortment due to female social organization.

Pacific Ocean–Wide Profile of CYP1A1 Expression, Stable Carbon and Nitrogen Isotope Ratios, and Organic Contaminant Burden in Sperm Whale Skin Biopsies

Background Ocean pollution affects marine organisms and ecosystems as well as humans. The International Oceanographic Commission recommends ocean health monitoring programs to investigate the presence of marine contaminants and the health of threatened species and the use of multiple and early-warning biomarker approaches. Objective We explored the hypothesis that biomarker and contaminant analyses in skin biopsies of the threatened sperm whale (Physeter macrocephalus) could reveal geographical trends in exposure on an oceanwide scale. Methods We analyzed cytochrome P450 1A1 (CYP1A1) expression (by immunohistochemistry), stable nitrogen and carbon isotope ratios (as general indicators of trophic position and latitude, respectively), and contaminant burdens in skin biopsies to explore regional trends in the Pacific Ocean. Results Biomarker analyses revealed significant regional differences within the Pacific Ocean. CYP1A1 expression was highest in whales from the Galapagos, a United Nations Educational, Scientific, and Cultural Organization World Heritage marine reserve, and was lowest in the sampling sites farthest away from continents. We examined the possible influence of the whales’ sex, diet, or range and other parameters on regional variation in CYP1A1 expression, but data were inconclusive. In general, CYP1A1 expression was not significantly correlated with contaminant burdens in blubber. However, small sample sizes precluded detailed chemical analyses, and power to detect significant associations was limited. Conclusions Our large-scale monitoring study was successful at identifying regional differences in CYP1A1 expression, providing a baseline for this known biomarker of exposure to aryl hydrocarbon receptor agonists. However, we could not identify factors that explained this variation. Future oceanwide CYP1A1 expression profiles in cetacean skin biopsies are warranted and could reveal whether globally distributed chemicals occur at biochemically relevant concentrations on a global basis, which may provide a measure of ocean integrity.

Global Assessment of Silver Pollution using Sperm Whales (Physeter macrocephalus) as an Indicator Species

Silver pollution in the marine environment is of concern, particularly, with the rapid increasing use of silver nanoparticles in consumer products providing additional sources of silver emissions. Silver is highly toxic and known to bioaccumulate in aquatic organisms; however, the risk silver poses to the marine ecosystem is poorly understood. The sperm whale (Physeter macrocephalus), a toothed whale having a wide global distribution and high trophic level, is a sentinel of ocean health. The aim of this study was to provide a global baseline for silver as a marine pollutant using the sperm whale as an indicator species. Skin biopsies were collected in free-ranging sperm whales around the globe during the voyage of the research vessel, Odyssey, during 2000 and 2005. Total silver levels were measured in 298 sperm whales from 16 regions. Detectable levels were found in 176 whales and ranged from 0.1 to 4,179.0 μg/g ww with a global mean level of 16.9 ± 14.1 μg/g ww. The highest mean level was found in whales sampled in waters near Seychelles with 123.3 μg/g ww, and the lowest mean in whales near Chagos with 0.1 μg/g ww. These data provide an important global baseline for silver pollution that precedes the recent emergence of silver nanoparticles.

A Global Assessment of Gold, Titanium, Strontium and Barium Pollution Using Sperm Whales (Physeter Macrocephalus) As an Indicator Species

This study provides a global baseline for barium, gold, titanium and strontium as marine pollutants using the sperm whale (Physeter macrocephalus) as an indicator species. Barium, gold, titanium and strontium are metals that are little studied in marine environments. However, their recent emergence as nanomaterials will likely increase their presence in the marine environment. Moreover, nanosized particles are likely to exhibit toxic outcomes not seen in macrosized particles. Biopsies from free ranging sperm whales were collected from around the globe. Total barium levels were measured in 275 of 298 sperm whales tested for barium and collected from 16 regions around the globe. The global mean for barium was 0.93 +/- 0.2ug/g with a detectable range from 0.1 to 27.9ug. Total strontium levels were measurable in all 298 sperm whales producing a global mean level of 2.2 +/- 0.1ug/g and a range from 0.2 to 11.5ug/g. Total titanium levels were also measured in all 298 sperm whales producing a global mean level of 4.5 +/- 0.25ug/g with a range from 0.1 to 29.8ug/g. Total gold levels were detected in 50 of the 194 sperm whales collected from 16 regions around the globe. Detectable levels ranged from 0.1 to 2.3ug/g tissue with a global mean level equal to 0.2 +/- 0.02ug/g. Previous reports of these metals were much lower than the mean levels reported here. The likely explanation is location differences and consistent with this explanation, we found statistically significant variation among regions. These data provide an important global baseline for barium, gold, titanium and strontium pollution and will allow for important comparisons to be made over time to assess the impact of nanomaterials on whales and the marine environment.

Crowdsourcing Modern and Historical Data Identifies Sperm Whale (Physeter macrocephalus) Habitat Offshore of South-Western Australia

The distribution and use of pelagic habitat by sperm whales (Physeter macrocephalus) is poorly understood in the south-eastern Indian Ocean off Western Australia. However, a variety of data are available via online portals where records of historical expeditions, commercial whaling operations, and modern scientific research voyages can now be accessed. Crowdsourcing these online data allows collation of presence-only information of animals and provides a valuable tool to help augment areas of low research effort. Four data sources were examined, the primary one being the Voyage of the Odyssey expedition, a five-year global study of sperm whales and ocean pollution. From December 2001-May 2002, acoustic surveys were conducted along 5,200 nautical miles of transects off Western Australia including the Perth Canyon and historical whaling grounds off Albany; 60 tissue biopsy samples were also collected. To augment areas not surveyed by the RV Odyssey, historical Yankee whaling data (1712-1920), commercial whaling data (1904-1999), and citizen science reports of sperm whale sightings (1990-2003) were used. Using Maxent, a species distribution modeling tool, we found that the submarine canyons off Albany and Perth provide important habitat for sperm whales. Current technology, along with current understanding of sperm whale bioacoustics and habitat preferences, provides strong motivation for undertaking long-term passive acoustic studies that can monitor the sperm whale population within Australia’s EEZ waters (Perth and Albany canyons) as a way of informing future marine management and policy decisions.