Peter S. Ross

Science and policy on endocrine disrupters must not be mixed: a reply to a “common sense” intervention by toxicology journal editors

The “common sense” intervention by toxicology journal editors regarding proposed European Union endocrine disrupter regulations ignores scientific evidence and well-established principles of chemical risk assessment. In this commentary, endocrine disrupter experts express their concerns about a recently published, and is in our considered opinion inaccurate and factually incorrect, editorial that has appeared in several journals in toxicology. Some of the shortcomings of the editorial are discussed in detail. We call for a better founded scientific debate which may help to overcome a polarisation of views detrimental to reaching a consensus about scientific foundations for endocrine disrupter regulation in the EU.

High PCB Concentrations in Free-Ranging Pacific Killer Whales, Orcinus orca: Effects of Age, Sex and Dietary Preference

Blubber biopsy samples were obtained for contaminant analysis from two discrete populations of killer whales (Orcinus orca) which frequent the coastal waters of British Columbia, Canada. Detailed life history information for the fish-eating ‘resident’ population, comprising two distinct communities, and the marine mammal-eating ‘transient’ killer whale population, provided an invaluable reference for the interpretation of contaminant concentrations. Total PCB concentrations (sum of 136 congeners detected) were surprisingly high in all three communities, but transient killer whales were particularly contaminated. PCB concentrations increased with age in males, but were greatly reduced in reproductively active females. The absence of age, sex and inter-community diAerences in concentrations of polychlorinated- dibenzo-p-dioxins (PCDDs) and- dibenzofurans (PCDFs) may have partly reflected low dietary levels, but more importantly, metabolic removal of dioxin-like compounds in killer whales. While information on toxic thresholds does not exist for PCBs in cetaceans, total 2,3,7,8-TCDD Toxic Equivalents (TEQ) in most killer whales sampled easily surpassed adverse eAects levels established for harbour seals, suggesting that the majority of free-ranging killer whales in this region are at risk for toxic eAects. The southern resident and transient killer whales of British Columbia can now be considered among the most contaminated cetaceans in the world. ” 2000 Elsevier Science Ltd. All rights reserved.

Contaminant-induced immunotoxicity in harbour seals: wildlife at risk?

Persistent, lipophilic polyhalogenated aromatic hydrocarbons (PHAHs) accumulate readily in the aquatic food chain and are found in high concentrations in seals and other marine mammals. Recent mass mortalities among several marine mammal populations have been attributed to infection by morbilliviruses, but a contributing role for immunotoxic PHAHs, including the polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs), and polychlorinated dibenzofurans (PCDFs) was not ruled out. We addressed this issue by carrying out a semi-field study in which captive harbour seals were fed herring from either the relatively uncontaminated Atlantic Ocean or the contaminated Baltic Sea for 2 years. We present here an overview of results obtained during this study. An impairment of natural killer (NK) cell activity, in vitro T-lymphocyte function, antigen-specific in vitro lymphocyte proliferative responses, and in vivo delayed-type hypersensitivity and antibody responses to ovalbumin was observed in the seals fed the contaminated Baltic herring. Additional feeding studies in PVG rats using the same herring batches suggested that an effect at the level of the thymus may be responsible for changes in cellular immunity, that virus-specific immune responses may be impaired, and that perinatal exposure to environmental contaminants represents a greater immunotoxic threat than exposure as a juvenile or adult. Together with the pattern of TCDD toxic equivalents of different PHAHs in the herring, these data indicate that present levels of PCBs in the aquatic food chain are immunotoxic to mammals. A review of contaminant levels in free-ranging harbour seals inhabiting polluted areas of Europe and North America suggests that many populations may be at risk to immunotoxicity. This could result in diminished host resistance and an increased incidence and severity of infectious disease.

Olfactory toxicity in fishes

Olfaction conveys critical environmental information to fishes, enabling activities such as mating, locating food, discriminating kin, avoiding predators and homing. All of these behaviors can be impaired or lost as a result of exposure to toxic contaminants in surface waters. Historically, teleost olfaction studies have focused on behavioral responses to anthropogenic contaminants (e.g., avoidance). More recently, there has been a shift towards understanding the underlying mechanisms and functional significance of contaminant-mediated changes in fish olfaction. This includes a consideration of how contaminants affect the olfactory nervous system and, by extension, the downstream physiological and behavioral processes that together comprise a normal response to naturally occurring stimuli (e.g., reproductive priming or releasing pheromones). Numerous studies spanning several species have shown that ecologically relevant exposures to common pollutants such as metals and pesticides can interfere with fish olfaction and disrupt life history processes that determine individual survival and reproductive success. This represents one of the pathways by which toxic chemicals in aquatic habitats may increasingly contribute to the decline and at-risk status of many commercially and ecologically important fish stocks. Despite our emerging understanding of the threats that pollution poses for chemical communication in aquatic communities, many research challenges remain. These include: (1) the determination of specific mechanisms of toxicity in the fish olfactory sensory epithelium; (2) an understanding of the impacts of complex chemical mixtures; (3) the capacity to assess olfactory toxicity in fish in situ; (4) the impacts of toxins on olfactory-mediated behaviors that are still poorly understood for many fish species; and (5) the connections between sublethal effects on individual fish and the long-term viability of wild populations. This review summarizes and integrates studies on fish olfaction-contaminant interactions, including metrics ranging from the molecular to the behavioral, and highlights directions for future research.

Widespread distribution of microplastics in subsurface seawater in the NE Pacific Ocean.

We document the abundance, composition and distribution of microplastics in sub-surface seawaters of the northeastern Pacific Ocean and coastal British Columbia. Samples were acid-digested and plastics were characterized using light microscopy by type (fibres or fragments) and size (<100, 100-500, 500-100 and >1000 μm). Microplastics concentrations ranged from 8 to 9200 particles/m(3); lowest concentrations were in offshore Pacific waters, and increased 6, 12 and 27-fold in west coast Vancouver Island, Strait of Georgia, and Queen Charlotte Sound, respectively. Fibres accounted for ∼ 75% of particles on average, although nearshore samples had more fibre content than offshore (p<0.05). While elevated microplastic concentrations near urban areas are consistent with land-based sources, the high levels in Queen Charlotte Sound appeared to be the result of oceanographic conditions that trap and concentrate debris. This assessment of microplastics in the NE Pacific is of interest in light of the on-coming debris from the 2011 Tohoku Tsunami.

Large and growing environmental reservoirs of Deca-BDE present an emerging health risk for fish and marine mammals

Polybrominated diphenyl ethers (PBDEs) have been the subject of intense scientific and regulatory scrutiny during recent years. Of the three commercial forms (Penta, Octa and Deca) of PBDEs that have been widely used as flame retardants in textiles, furniture upholstery, plastics, and electronics, only Deca-BDE remains on the general market in North America, while a recent ruling of the European Court spells an impending end to its use in Europe. We review here highlights of aquatic research documenting the rapid emergence of PBDEs as a high priority environmental concern in Canada. PBDEs are being introduced in large quantities to the aquatic environment through sewage discharge and atmospheric deposition. In certain environmental compartments, the single congener BDE-209, the main ingredient in the Deca-BDE formulation, has surpassed the legacy PCBs and DDT as the top contaminant by concentration. Limited biomagnification of BDE-209 in aquatic food webs reflects its high log K(ow) and preferential partitioning into the particle phase. As a result, large environmental reservoirs of BDE-209 are being created in sediments, and these may present a long-term threat to biota: BDE-209 breaks down into more persistent, more bioaccumulative, more toxic, and more mobile PBDE congeners in the environment.

Suppression of natural killer cell activity in harbour seals (Phoca vitulina) fed Baltic Sea herring

Mass mortalities among marine mammal populations in recent years have raised questions about a possible contributory role of contaminants accumulated through the marine food chain. While viruses were shown to be the primary cause of the outbreaks, an immunotoxic action by organochlorine chemicals in affected animals could not be ruled out. We carried out a 212-year immunotoxicological experiment in which two groups of 11 harbour seals each were fed herring from either the relatively contaminated Baltic Sea or the relatively uncontaminated Atlantic Ocean. Seals in the Baltic Sea group accumulated 3–4 times higher levels of Ah-receptor-mediated 2,3,7,8-TCDD Toxic Equivalents in blubber than did their Atlantic counterparts following 2 years on the respective diets. Blood was sampled a total of 17 times during the course of the experiment for immunological evaluation, during which time the natural cytotoxic activity of peripheral blood mononuclear cells isolated from seals fed Baltic Sea herring declined to a level approximately 25% lower than that observed in seals fed Atlantic herring (P < 0.01). Natural killer (NK) cell activity has not been previously described for a marine mammal species. We characterized the natural cytotoxic activity of harbour seal peripheral blood mononuclear cells (PBMC), and found this to be interleukin-2 (IL-2) responsive, sensitive to antibody anti-asialo GM1, and it was higher against a virus-infected target cell, like NK cells described for other mammals. As NK cells are leukocytes which play an important role in the first line of defence against viruses, the observed impairment of NK cell activity in the seals feeding on the Baltic Sea herring suggests that exposure to contaminants may have an adverse effect on the defence against virus infections in seals inhabiting polluted waters in Europe. This may therefore have affected the severity of the infections, the survival rates and the spread of infections during recent epizootics.

Marine Mammals as Sentinels in Ecological Risk Assessment

As high trophic level organisms in the marine environment, fish-eating seals, dolphins and whales are often exposed to very high levels of fat-soluble environmental contaminants. Assessing the sources, levels and patterns of contaminants found in the tissues of marine mammals, and the biological effects of these contaminants on individuals, is essential to determining any population- or species-level impacts. While the number of contaminants to which marine mammals are exposed is staggering, designing strategies to assess the effects of complex mixtures represent a challenging yet vital part of an understanding of the “real world”. At present, an accumulated “weight of evidence” suggests that ambient levels of lipophilic contaminants have adversely affected aspects of reproduction, immune function and endocrine function in marine mammals inhabiting a number of industrial coastal regions. This body of evidence is drawn from a combination of (1) epidemiological or descriptive studies of effects observed in free-ranging populations of marine mammals inhabiting contaminated areas; (2) mechanistic, cause-and-effect, laboratory rodent studies, using single- or multiple- chemical exposures in acute or chronic designs; (3) semi-field or captive studies of marine mammals fed fish from contaminated areas; and (4) laboratory studies where rodent species are used as surrogates for marine mammals, and are exposed to extracts of complex contaminant mixtures found in fish. While these approaches have been used to delineate the effects of historically introduced environmental contaminants such as PCBs and DDT on wildlife, they may serve to identify the ecological risks presented by (1) the continued leaking of stored, discontinued, chemical supplies that have not yet been destroyed (e.g., PCBs); (2) new chemicals that may have lipophilic or persistent characteristics similar to those found currently in marine mammals; and (3) diet selection as a source of contaminants for humans, since certain human groups share the same food chain with marine mammals. Contaminant mixtures to which marine mammals are exposed differ greatly from the original industrial mixtures as a result of differing rates of accumulation and capacities to metabolize certain chemical types by the various trophic levels (e.g., invertebrates, fish, and marine mammals) of the food chain. Marine mammals ultimately provide information on the chemicals which present the greatest risk to consumers at the top of the food chain, something that cannot be adequately described or predicted in laboratory models.

PCB-related alteration of thyroid hormones and thyroid hormone receptor gene expression in free-ranging harbor seals (Phoca vitulina)

Persistent organic pollutants are environmental contaminants that, because of their lipophilic properties and long half-lives, bioaccumulate within aquatic food webs and often reach high concentrations in marine mammals, such as harbor seals (Phoca vitulina). Exposure to these contaminants has been associated with developmental abnormalities, immunotoxicity, and reproductive impairment in marine mammals and other high-trophic-level wildlife, mediated via a disruption of endocrine processes. The highly conserved thyroid hormones (THs) represent one vulnerable endocrine end point that is critical for metabolism, growth, and development in vertebrates. We characterized the relationship between contaminants and specific TH receptor (TR ) gene expression in skin/blubber biopsy samples, as well as serum THs, from free-ranging harbor seal pups (n = 39) in British Columbia, Canada, and Washington State, USA. We observed a contaminant-related increase in blubber TR-α gene expression [total polychlorinated biphenyls (∑PCBs); r = 0.679; p < 0.001] and a concomitant decrease in circulating total thyroxine concentrations (∑PCBs; r = −0.711; p < 0.001). Consistent with results observed in carefully controlled laboratory and captive feeding studies, our findings suggest that the TH system in harbor seals is highly sensitive to disruption by environmental contaminants. Such a disruption not only may lead to adverse effects on growth and development but also could have important ramifications for lipid metabolism and energetics in marine mammals.

Harbor seals (Phoca vitulina) in British Columbia, Canada, and Washington State, USA, reveal a combination of local and global polychlorinated biphenyl, dioxin, and furan signals

The harbor seal (Phoca vitulina) can serve as a useful indicator of food web contamination by persistent organic pollutants (POPs) because of its high trophic level, wide distribution in temperate coastal waters of the Northern Hemisphere, and relative ease of capture. In 1996 through 1997, we live-captured 60 harbor seal pups from three regions, spanning remote (Queen Charlotte Strait, BC, Canada), moderately industrialized (Strait of Georgia, BC, Canada), and heavily industrialized (Puget Sound, WA, USA) marine basins straddling the Canada-United States border. Biopsy samples of blubber were taken and analyzed for congener-specific polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs), and polychlorinated dibenzofurans (PCDFs) by using high-resolution gas chromatography-high-resolution mass spectrometry. Harbor seals in Puget Sound were heavily contaminated with PCBs, whereas seals from the Strait of Georgia had relatively high concentrations of PCDDs and PCDFs. Pattern evaluation and principal components analysis suggested that proximity to sources influenced the mixture to which seals were exposed, with those inhabiting more remote areas being exposed to lighter PCB congeners (those with lower Henrys law constant and K(ow)) that disperse more readily through atmospheric and other processes. Total toxic equivalents to 2,3,7,8-tetrachlorodibenzo-p-dioxin for the PCBs, PCDDs, and PCDFs suggest that Puget Sound seals are at greatest risk for adverse health effects, and that PCBs represent the class of dioxinlike contaminants of greatest concern at all sites.