Dietary Exposure to Environmentally Relevant Levels of Chemical Contaminants Reduces Growth and Survival in Juvenile Chinook Salmon.

Chemical pollution can degrade aquatic ecosystems. Chinook salmon in contaminated habitats are vulnerable to health impacts from toxic exposures. Few studies have been conducted on adverse health outcomes associated with current levels and mixtures of contaminants. Fewer still address effects specific to the juvenile life-stage of salmonids. The present study evaluated contaminant-related effects from dietary exposure to environmentally relevant concentrations and mixture profiles in juvenile Chinook salmon from industrialized waterways in the U.S. Pacific Northwest using two end points: growth assessment and disease susceptibility. The dose and chemical proportions were reconstituted based on environmental sampling and analysis using the stomach contents of juvenile Chinook salmon recently collected from contaminated, industrialized waterways. Groups of fish were fed a mixture with fixed proportions of 10 polychlorinated biphenyls (PCBs), 3 dichlorodiphenyltrichloroethanes (DDTs), and 13 polycyclic aromatic hydrocarbons (PAHs) at five concentrations for 35 days. These contaminant compounds were selected because of elevated concentrations and the widespread presence in sediments throughout industrialized waterways. Fork length and otolith microstructural growth indicators were significantly reduced in fish fed environmentally relevant concentrations of these contaminants. In addition, contaminant-exposed Chinook salmon were more susceptible to disease during controlled challenges with the pathogen Aeromonas salmonicida. Our results indicate that dietary exposure to contaminants impairs growth and immune function in juvenile Chinook salmon, thereby highlighting that current environmental exposure to chemicals of potential management concern threatens the viability of exposed salmon.

A comprehensive petrochemical vulnerability index for marine fishes in the Gulf of Mexico.

Oil and gas extraction activities occur across the globe, yet species-specific toxicological information on the biological and ecological impacts of exposure to petrochemicals is lacking for the vast majority of marine species. To help prioritize species for recovery, mitigation, and conservation in light of significant toxicological data gaps, a trait-based petrochemical vulnerability index was developed and applied to the more than 1700 marine fishes present across the entire Gulf of Mexico, including all known bony fishes, sharks, rays and chimaeras. Using life history and other traits related to likelihood of exposure, physiological sensitivity to exposure, and population resiliency, final calculated petrochemical vulnerability scores can be used to provide information on the relative sensitivity, or resilience, of marine fish populations across the Gulf of Mexico to oil and gas activities. Based on current knowledge of traits, marine fishes with the highest vulnerability scores primarily occur in areas of high petrochemical activity, are found at or near the surface, and have low reproductive turnover rates and/or highly specialized diet and habitat requirements. Relative population vulnerability scores for marine fishes can be improved with additional toxicokinetic studies, including those that account for the synergistic or additive effect of multiple stressors, as well as increased research on ecological and life history traits, especially for deep living species.

A review of the toxicology of oil in vertebrates: what we have learned following the Deepwater Horizon oil spill.

In the wake of the Deepwater Horizon (DWH) oil spill, a number of government agencies, academic institutions, consultants, and nonprofit organizations conducted lab- and field-based research to understand the toxic effects of the oil. Lab testing was performed with a variety of fish, birds, turtles, and vertebrate cell lines (as well as invertebrates); field biologists conducted observations on fish, birds, turtles, and marine mammals; and epidemiologists carried out observational studies in humans. Eight years after the spill, scientists and resource managers held a workshop to summarize the similarities and differences in the effects of DWH oil on vertebrate taxa and to identify remaining gaps in our understanding of oil toxicity in wildlife and humans, building upon the cross-taxonomic synthesis initiated during the Natural Resource Damage Assessment. Across the studies, consistency was found in the types of toxic response observed in the different organisms. Impairment of stress responses and adrenal gland function, cardiotoxicity, immune system dysfunction, disruption of blood cells and their function, effects on locomotion, and oxidative damage were observed across taxa. This consistency suggests conservation in the mechanisms of action and disease pathogenesis. From a toxicological perspective, a logical progression of impacts was noted: from molecular and cellular effects that manifest as organ dysfunction, to systemic effects that compromise fitness, growth, reproductive potential, and survival. From a clinical perspective, adverse health effects from DWH oil spill exposure formed a suite of signs/symptomatic responses that at the highest doses/concentrations resulted in multi-organ system failure.

A multi-taxonomic framework for assessing relative petrochemical vulnerability of marine biodiversity in the Gulf of Mexico.

A fundamental understanding of the impact of petrochemicals and other stressors on marine biodiversity is critical for effective management, restoration, recovery, and mitigation initiatives. As species-specific information on levels of petrochemical exposure and toxicological response are lacking for the majority of marine species, a trait-based assessment to rank species vulnerabilities to petrochemical activities in the Gulf of Mexico can provide a more comprehensive and effective means to prioritize species, habitats, and ecosystems for improved management, restoration and recovery. To initiate and standardize this process, we developed a trait-based framework, applicable to a wide range of vertebrate and invertebrate species, that can be used to rank relative population vulnerabilities of species to petrochemical activities in the Gulf of Mexico. Through expert consultation, 18 traits related to likelihood of exposure, individual sensitivity, and population resilience were identified and defined. The resulting multi-taxonomic petrochemical vulnerability framework can be adapted and applied to a wide variety of species groups and geographic regions. Additional recommendations and guidance on the application of the framework to rank species vulnerabilities under specific petrochemical exposure scenarios, management needs or data limitations are also discussed.

Severe thiamine deficiency in eastern Baltic cod (Gadus morhua).

The eastern Baltic cod (Gadus morhua) population has been decreasing in the Baltic Sea for at least 30 years. Condition indices of the Baltic cod have decreased, and previous studies have suggested that this might be due to overfishing, predation, lower dissolved oxygen or changes in salinity. However, numerous studies from the Baltic Sea have demonstrated an ongoing thiamine deficiency in several animal classes, both invertebrates and vertebrates. The thiamine status of the eastern Baltic cod was investigated to determine if thiamine deficiency might be a factor in ongoing population declines. Thiamine concentrations were determined by chemical analyses of thiamine, thiamine monophosphate and thiamine diphosphate (combined SumT) in the liver using high performance liquid chromatography. Biochemical analyses measured the activity of the thiamine diphosphate-dependent enzyme transketolase to determine the proportion of apoenzymes in both liver and brain tissue. These biochemical analyses showed that 77% of the cod were thiamine deficient in the liver, of which 13% had a severe thiamine deficiency (i.e. 25% transketolase enzymes lacked thiamine diphosphate). The brain tissue of 77% of the cod showed thiamine deficiency, of which 64% showed severe thiamine deficiency. The thiamine deficiency biomarkers were investigated to find correlations to different biological parameters, such as length, weight, otolith weight, age (annuli counting) and different organ weights. The results suggested that thiamine deficiency increased with age. The SumT concentration ranged between 2.4-24 nmol/g in the liver, where the specimens with heavier otoliths had lower values of SumT (P = 0.0031). Of the cod sampled, only 2% of the specimens had a Fulton's condition factor indicating a healthy specimen, and 49% had a condition factor below 0.8, indicating poor health status. These results, showing a severe thiamine deficiency in eastern Baltic cod from the only known area where spawning presently occurs for this species, are of grave concern.

Transcriptional changes in innate immunity genes in head kidneys from Aeromonas salmonicida-challenged rainbow trout fed a mixture of polycyclic aromatic hydrocarbons.

We previously observed that exposure to a complex mixture of high molecular weight polycyclic aromatic hydrocarbons (PAHs) increased sensitivity of rainbow trout (Oncorhynchus mykiss) to subsequent challenge with Aeromonas salmonicida, the causative agent of furunculosis. In this study, we evaluate potential mechanisms associated with disease susceptibility from combined environmental factors of dietary PAH exposure and pathogen challenge. Rainbow trout were fed a mixture of ten high molecular weight PAHs at an environmentally relevant concentration (7.82µg PAH mixture/g fish/day) or control diet for 50 days. After 50 days of PAH exposure, fish were challenged with either Aeromonas salmonicida at a lethal concentration 30 (LC30) or growth media without the pathogen (mock challenge). Head kidneys were collected 2, 4, 10 and 20 days after challenge and gene expression (q<0.05) was evaluated among treatments. In animals fed the PAH contaminated diet, we observed down-regulation of expression for innate immune system genes in pathways (p<0.05) for the terminal steps of the complement cascade (complement component C6) and other bacteriolytic processes (lysozyme type II) potentially underlying increased disease susceptibility after pathogen challenge. Increased expression of genes associated with hemorrhage/tissue remodeling/inflammation pathways (p<0.05) was likely related to more severe head kidney damage due to infection in PAH-fed compared to control-fed fish. This study is the first to evaluate transcriptional signatures associated with the impact of chronic exposure to an environmentally relevant mixture of PAHs in disease susceptibility and immunity.

A Conceptual Model to Assess Stress-Associated Health Effects of Multiple Ecosystem Services Degraded by Disaster Events in the Gulf of Mexico and Elsewhere.

Few conceptual frameworks attempt to connect disaster-associated environmental injuries to impacts on ecosystem services (the benefits humans derive from nature) and thence to both psychological and physiological human health effects. To our knowledge, this study is one of the first, if not the first, to develop a detailed conceptual model of how degraded ecosystem services affect cumulative stress impacts on the health of individual humans and communities. Our comprehensive Disaster-Pressure State-Ecosystem Services-Response-Health (DPSERH) model demonstrates that oil spills, hurricanes, and other disasters can change key ecosystem components resulting in reductions in individual and multiple ecosystem services that support people's livelihoods, health, and way of life. Further, the model elucidates how damage to ecosystem services produces acute, chronic, and cumulative stress in humans which increases risk of adverse psychological and physiological health outcomes. While developed and initially applied within the context of the Gulf of Mexico, it should work equally well in other geographies and for many disasters that cause impairment of ecosystem services. Use of this new tool will improve planning for responses to future disasters and help society more fully account for the costs and benefits of potential management responses. The model also can be used to help direct investments in improving response capabilities of the public health community, biomedical researchers, and environmental scientists. Finally, the model illustrates why the broad range of potential human health effects of disasters should receive equal attention to that accorded environmental damages in assessing restoration and recovery costs and time frames.

Widespread episodic thiamine deficiency in Northern Hemisphere wildlife.

Many wildlife populations are declining at rates higher than can be explained by known threats to biodiversity. Recently, thiamine (vitamin B1) deficiency has emerged as a possible contributing cause. Here, thiamine status was systematically investigated in three animal classes: bivalves, ray-finned fishes, and birds. Thiamine diphosphate is required as a cofactor in at least five life-sustaining enzymes that are required for basic cellular metabolism. Analysis of different phosphorylated forms of thiamine, as well as of activities and amount of holoenzyme and apoenzyme forms of thiamine-dependent enzymes, revealed episodically occurring thiamine deficiency in all three animal classes. These biochemical effects were also linked to secondary effects on growth, condition, liver size, blood chemistry and composition, histopathology, swimming behaviour and endurance, parasite infestation, and reproduction. It is unlikely that the thiamine deficiency is caused by impaired phosphorylation within the cells. Rather, the results point towards insufficient amounts of thiamine in the food. By investigating a large geographic area, by extending the focus from lethal to sublethal thiamine deficiency, and by linking biochemical alterations to secondary effects, we demonstrate that the problem of thiamine deficiency is considerably more widespread and severe than previously reported.

Environmental effects of the Deepwater Horizon oil spill: A review.

The Deepwater Horizon oil spill constituted an ecosystem-level injury in the northern Gulf of Mexico. Much oil spread at 1100-1300m depth, contaminating and affecting deepwater habitats. Factors such as oil-biodegradation, ocean currents and response measures (dispersants, burning) reduced coastal oiling. Still, >2100km of shoreline and many coastal habitats were affected. Research demonstrates that oiling caused a wide range of biological effects, although worst-case impact scenarios did not materialize. Biomarkers in individual organisms were more informative about oiling stress than population and community indices. Salt marshes and seabird populations were hard hit, but were also quite resilient to oiling effects. Monitoring demonstrated little contamination of seafood. Certain impacts are still understudied, such as effects on seagrass communities. Concerns of long-term impacts remain for large fish species, deep-sea corals, sea turtles and cetaceans. These species and their habitats should continue to receive attention (monitoring and research) for years to come.

Aluminum smelter-derived polycyclic aromatic hydrocarbons and flatfish health in the Kitimat marine ecosystem, British Columbia, Canada.

From 2000-2004 a monitoring study was conducted to evaluate the impacts of aluminum smelter-derived polycyclic aromatic hydrocarbons (PAHs) on the health of fish in the marine waters of Kitimat, British Columbia, Canada. These waters are part of the historical fishing grounds of the Haisla First Nation, and since the 1950s the Alcan Primary Metal Company has operated an aluminum smelter at the head of the Kitimat Arm embayment. As a result, adjacent marine and estuarine sediments have been severely contaminated with a mixture of smelter-associated PAHs in the range of 10,000-100,000 ng/g dry wt. These concentrations are above those shown to cause adverse effects in fish exposed to PAHs in urban estuaries, but it was uncertain whether comparable effects would be seen at the Kitimat site due to limited bioavailability of smelter-derived PAHs. Over the 5-year study we conducted biennial collections of adult English sole (Parophrys vetulus) and sediment samples at the corresponding capture sites. Various tissue samples (e.g. liver, kidney, gonad, stomach contents) and bile were taken from each animal to determine levels of exposure and biological effects, and compare the uptake and toxicity of smelter-derived PAHs with urban mixtures of PAHs. Results showed significant intersite differences in concentrations of PAHs. Sole collected at sites nearest the smelter showed increased PAH exposure, as well as significantly higher prevalences of PAH-associated liver disease, compared to sites within Kitimat Arm that were more distant from the smelter. However, measures of PAH exposure (e.g., bile metabolites) were surprisingly high in sole from the reference sites outside of Kitimat Arm, though sediment and dietary PAHs at these sites were low, and fish from the areas showed no biological injury. PAH uptake, exposure, and biological effects in Kitimat English sole were relatively lower when compared to English sole collected from urban sites contaminated with PAH mixtures from other sources. These findings indicate that while smelter-associated PAHs in Kitimat Arm appear to be causing some injury to marine resources, they likely have reduced bioavailability, and thus reduced biological toxicity, compared to other environmental PAH mixtures.

Health of common bottlenose dolphins ( Tursiops truncatus ) in Barataria Bay, Louisiana, following the deepwater horizon oil spill.

The oil spill resulting from the explosion of the Deepwater Horizon drilling platform initiated immediate concern for marine wildlife, including common bottlenose dolphins in sensitive coastal habitats. To evaluate potential sublethal effects on dolphins, health assessments were conducted in Barataria Bay, Louisiana, an area that received heavy and prolonged oiling, and in a reference site, Sarasota Bay, Florida, where oil was not observed. Dolphins were temporarily captured, received a veterinary examination, and were then released. Dolphins sampled in Barataria Bay showed evidence of hypoadrenocorticism, consistent with adrenal toxicity as previously reported for laboratory mammals exposed to oil. Barataria Bay dolphins were 5 times more likely to have moderate-severe lung disease, generally characterized by significant alveolar interstitial syndrome, lung masses, and pulmonary consolidation. Of 29 dolphins evaluated from Barataria Bay, 48% were given a guarded or worse prognosis, and 17% were considered poor or grave, indicating that they were not expected to survive. Disease conditions in Barataria Bay dolphins were significantly greater in prevalence and severity than those in Sarasota Bay dolphins, as well as those previously reported in other wild dolphin populations. Many disease conditions observed in Barataria Bay dolphins are uncommon but consistent with petroleum hydrocarbon exposure and toxicity.

Endocrine disrupting chemicals in fish bile: a rapid method of analysis using English sole (Parophrys vetulus) from Puget Sound, WA, USA.

This study describes a recently developed and rapid method to measure bisphenol A (BPA), 17ß-estradiol (E2) and 17α-ethynylestradiol (EE2) in bile of fish using enzymatic hydrolysis of samples followed by solid-phase extraction and ultra-performance liquid chromatography with tandem mass spectrometry. The limits of quantitation (LOQ) for BPA, EE2 and E2 were 6.3ngmL(-1), 12.5ngmL(-1) and 6.3ngmL(-1), respectively. These compounds were analyzed in bile of male English sole (Parophrys vetulus) collected from urban and non-urban sites in Puget Sound, WA, USA. The BPA and E2 concentrations (and occurrence) ranged from

A perspective on the history and evolution of an Oceans and Human Health "metadiscipline" in the USA.

We review recent history and evolution of Oceans and Human Health programs and related activities in the USA from a perspective within the Federal government. As a result of about a decade of support by the US Congress and through a few Federal agencies, notably the National Science Foundation, National Institute of Environmental Health Sciences, and National Ocean and Atmospheric Administration, robust Oceans and Human Health (OHH) research and application activities are now relatively widespread, although still small, in a number of agencies and academic institutions. OHH themes and issues have been incorporated into comprehensive federal ocean research plans and are reflected in the new National Ocean Policy enunciated by Executive Order 13547. In just a decade, OHH has matured into a recognized "metadiscipline," with development of a small, but robust and diverse community of science and practice, incorporation into academic educational programs, regular participation in ocean and coastal science and public health societies, and active engagement with public health decision makers. In addition to substantial increases in scientific information, the OHH community has demonstrated ability to respond rapidly and effectively to emergency situations such as those associated with extreme weather events (e.g., hurricanes, floods) and human-caused disasters (e.g., the Deep Water Horizon oil spill). Among many other things, next steps include development and implementation of agency health strategies and provision of specific services, such as ecological forecasts to provide routine early warnings for ocean health threats and opportunities for prevention and mitigation of these risks.

Potent phototoxicity of marine bunker oil to translucent herring embryos after prolonged weathering.

Pacific herring embryos (Clupea pallasi) spawned three months following the Cosco Busan bunker oil spill in San Francisco Bay showed high rates of late embryonic mortality in the intertidal zone at oiled sites. Dead embryos developed to the hatching stage (e.g. fully pigmented eyes) before suffering extensive tissue deterioration. In contrast, embryos incubated subtidally at oiled sites showed evidence of sublethal oil exposure (petroleum-induced cardiac toxicity) with very low rates of mortality. These field findings suggested an enhancement of oil toxicity through an interaction between oil and another environmental stressor in the intertidal zone, such as higher levels of sunlight-derived ultraviolet (UV) radiation. We tested this hypothesis by exposing herring embryos to both trace levels of weathered Cosco Busan bunker oil and sunlight, with and without protection from UV radiation. Cosco Busan oil and UV co-exposure were both necessary and sufficient to induce an acutely lethal necrotic syndrome in hatching stage embryos that closely mimicked the condition of dead embryos sampled from oiled sites. Tissue levels of known phototoxic polycyclic aromatic compounds were too low to explain the observed degree of phototoxicity, indicating the presence of other unidentified or unmeasured phototoxic compounds derived from bunker oil. These findings provide a parsimonious explanation for the unexpectedly high losses of intertidal herring spawn following the Cosco Busan spill. The chemical composition and associated toxicity of bunker oils should be more thoroughly evaluated to better understand and anticipate the ecological impacts of vessel-derived spills associated with an expanding global transportation network.

Unexpectedly high mortality in Pacific herring embryos exposed to the 2007 Cosco Busan oil spill in San Francisco Bay.

In November 2007, the container ship Cosco Busan released 54,000 gallons of bunker fuel oil into San Francisco Bay. The accident oiled shoreline near spawning habitats for the largest population of Pacific herring on the west coast of the continental United States. We assessed the health and viability of herring embryos from oiled and unoiled locations that were either deposited by natural spawning or incubated in subtidal cages. Three months after the spill, caged embryos at oiled sites showed sublethal cardiac toxicity, as expected from exposure to oil-derived polycyclic aromatic compounds (PACs). By contrast, embryos from the adjacent and shallower intertidal zone showed unexpectedly high rates of tissue necrosis and lethality unrelated to cardiotoxicity. No toxicity was observed in embryos from unoiled sites. Patterns of PACs at oiled sites were consistent with oil exposure against a background of urban sources, although tissue concentrations were lower than expected to cause lethality. Embryos sampled 2 y later from oiled sites showed modest sublethal cardiotoxicity but no elevated necrosis or mortality. Bunker oil contains the chemically uncharacterized remains of crude oil refinement, and one or more of these unidentified chemicals likely interacted with natural sunlight in the intertidal zone to kill herring embryos. This reveals an important discrepancy between the resolving power of current forensic analytical chemistry and biological responses of keystone ecological species in oiled habitats. Nevertheless, we successfully delineated the biological impacts of an oil spill in an urbanized coastal estuary with an overlapping backdrop of atmospheric, vessel, and land-based sources of PAC pollution.

Recurrent die-offs of adult coho salmon returning to spawn in Puget Sound lowland urban streams.

Several Seattle-area streams in Puget Sound were the focus of habitat restoration projects in the 1990s. Post-project effectiveness monitoring surveys revealed anomalous behaviors among adult coho salmon returning to spawn in restored reaches. These included erratic surface swimming, gaping, fin splaying, and loss of orientation and equilibrium. Affected fish died within hours, and female carcasses generally showed high rates (>90%) of egg retention. Beginning in the fall of 2002, systematic spawner surveys were conducted to 1) assess the severity of the adult die-offs, 2) compare spawner mortality in urban vs. non-urban streams, and 3) identify water quality and spawner condition factors that might be associated with the recurrent fish kills. The forensic investigation focused on conventional water quality parameters (e.g., dissolved oxygen, temperature, ammonia), fish condition, pathogen exposure and disease status, and exposures to metals, polycyclic aromatic hydrocarbons, and current use pesticides. Daily surveys of a representative urban stream (Longfellow Creek) from 2002-2009 revealed premature spawner mortality rates that ranged from 60-100% of each fall run. The comparable rate in a non-urban stream was <1% (Fortson Creek, surveyed in 2002). Conventional water quality, pesticide exposure, disease, and spawner condition showed no relationship to the syndrome. Coho salmon did show evidence of exposure to metals and petroleum hydrocarbons, both of which commonly originate from motor vehicles in urban landscapes. The weight of evidence suggests that freshwater-transitional coho are particularly vulnerable to an as-yet unidentified toxic contaminant (or contaminant mixture) in urban runoff. Stormwater may therefore place important constraints on efforts to conserve and recover coho populations in urban and urbanizing watersheds throughout the western United States.

Trends in organic pollutants and lipids in juvenile Snake River spring Chinook salmon with different outmigrating histories through the Lower Snake and Middle Columbia Rivers.

A three-year field study was conducted from 2006 to 2008 to monitor the spatial and temporal trends of organic pollutants in migrating juvenile Snake River spring Chinook salmon (Oncorhynchus tshawytscha) sampled from the Lower Snake and Middle Columbia River Basins. Specifically, hatchery-reared juvenile salmon were monitored as they navigated the Federal Columbia River Power System (FCRPS) by either transport barge (Barged) or remained in the river (In-River) from Lower Granite Dam to a terminal collection dam, either John Day Dam or Bonneville Dam. Levels of polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), and organochlorine (OC) pesticides were detected in the bodies of both In-River and Barged salmon during the 2006, 2007 and 2008 outmigrating season. At the terminal dam, In-River fish had greater concentrations of persistent organic pollutants POPs than Barged salmon. Of the POPs detected, dichlorodiphenyltrichloroethanes (DDTs) were found at the greatest concentrations in the salmon bodies. These elevated lipid-normalized concentrations in the In-River fish were due to lipid depletion in all years as well as increased exposure to POPs in some years as indicated by an increase in wet weight contaminant concentrations. Salmon were also exposed to polycyclic aromatic hydrocarbons (PAHs) as indicated by the phenanthrene (PHN) signal for biliary fluorescent aromatic compounds (FACs) at the hatcheries or prior to Lower Granite Dam. There were detectable levels of biliary FACs as fish migrated downstream or were barged to the terminal dam. Therefore, the potential exists for these organic pollutants and lipid levels to cause adverse effects and should be included as one of the variables to consider when examining the effects of the FCRPS on threatened and endangered juvenile salmon.