Contamination and toxic effects of persistent endocrine disrupters in marine mammals and birds

In recent years, several species of marine mammals and birds have been affected by uncommon diseases and unusual mortalities. While several possible causative factors have been attributed for these events, a prominent suspect is exposure to man-made toxic contaminants. Particularly, some of these man-made chemicals can disrupt normal endocrine physiology in animals. At CMES, our studies focus on exposure and toxic effects of endocrine disrupting chemicals, particularly organochlorines, in higher trophic level wildlife. Endocrine disrupting chemicals, such as organochlorine insecticides, polychlorinated biphenyls, organotins etc. are found in tissues of a wide variety of wildlife. Extremely high concentrations have been found in animals afflicted with diseases and/or victims of mass mortalities. Elevated contamination by organochlorines has been found in open sea animals such as cetaceans and albatrosses, which seemed to be attributable to their low capacity to metabolize toxic persistent contaminants. Significant correlations between biochemical parameters (serum hormone concentrations and cytochrome P450 enzyme activities) and residues of endocrine disrupting chemicals were found in some species of marine animals, which indicates that these chemicals may impose toxic effects in animals even at the current levels of exposure. In general, water birds and marine mammals accumulated the dioxin-like compounds with much higher concentrations than humans, implying higher risk from exposure in wildlife. The future issues of endocrine disrupting chemicals in humans and wildlife will have to be focused in developing countries.     

Ecological Significance of Endocrine Disruption in Marine Invertebrates

Anthropogenic chemicals which can disrupt the hormonal (endocrine) systems of wildlife species are currently a major cause for concern. Reproductive hormone-receptor systems appear to be especially vulnerable. In the past few years, numerous effects of endocrine disrupting chemicals on wildlife have emerged including changes in the sex of riverine fish, reproductive failure in birds and abnormalities in the reproductive organs of alligators and polar bears. Much less is known regarding endocrine disruption in marine invertebrates, the key structural and functional components of marine ecosystems.

In this paper, potential effects of different classes of endocrine disrupting chemicals are reviewed. The endocrinology of several major invertebrate groups is briefly examined to identify which phyla are most likely to be at risk. Gaps in our knowledge concerning the availability and uptake of endocrine disruptors are identified. For example, the relative importance of different routes of chemical uptake (from seawater vs food) is considered. Feeding strategies (herbivores, carnivores, deposit feeders, suspension feeders) in relation to uptake of endocrine disruptors are also discussed.

Examples of endocrine disruption in marine invertebrates in situ are provided, including imposex in gastropod molluscs exposed to organotin compounds and intersex in crustaceans exposed to sewage discharges. Laboratory data are presented concerning the effects of endocrine disruptors on the growth and reproductive output of the deposit feeding amphipod Corophium volutator and the polychaete worm Dinophilus gyrociliatus. Recent findings are reported which demonstrate reductions in settlement following exposure of barnacle larvae to the xeno-estrogen, 4 nonyl phenol. The potential use of cyprid major protein as a biomarker of oestrogenicity is explored. The ecological significance of endocrine disruption in marine invertebrates is discussed. With regard to environmental management action, an evidence-based approach is advocated. A protocol for collecting evidence of ecologically significant endocrine disruption is outlined.     

Endocrine Disrupters in the Aquatic Environment: An Overview

Although a relatively new area of environmental research, the field of endocrine disruption has grown very rapidly, and currently many hundreds, perhaps even a few thousand, papers are published annually on the many different aspects covered by the field. As far as endocrine disruption in wildlife is concerned, most attention has been focused on aquatic organisms, for two reasons. Firstly, the aquatic environment receives most of the pollutants intentionally released into the environment, through effluents from wastewater treatment plants, and secondly because many of the best documented examples of endocrine disruption in wildlife are of partially or completely aquatic species. These two reasons are probably not unconnected, of course. Hence, aquatic organisms can receive continuous exposure to endocrine‐disrupting chemicals throughout their lives, albeit usually to low concentrations of these chemicals. Analysis of effluents has identified many of the endocrine‐disrupting chemicals present, and shown that these are both natural and man‐made, and vary greatly in potency. Most attention has been directed to identifying the main estrogenic chemicals, because many of the effects reported in wildlife appear to be a consequence of ‘feminization’ of males. However, chemical analysis of effluents has also demonstrated that chemicals with other types of endocrine activity are present, such as androgens, anti‐androgens, progestagens, etc. The effects (if any, of course) of such chemicals on aquatic organisms are unknown, and largely uninvestigated, presently. Much of the biological research has centred on the effects of estrogenic chemicals, especially to fish. These effects, such as elevated vitellogenin concentrations and intersexuality, have to date been studied almost exclusively at the level of the individual, and hence whether endocrine‐disrupting chemicals cause population‐level consequences is largely unknown (the undeniable effects of TBT on molluscs, leading to local extinctions, being the exception). It is my opinion that rather too much of the recent research has not advanced our understanding of endocrine disruption a great deal, and we are probably not much further forward now than we were five years or so ago. It is surely time to tackle some of the outstanding, unresolved issues, such as the impact of endocrine disruption at the population level, and the issue of how organisms respond when exposed to complex mixtures of endocrine active chemicals. Such research will not be easy, and will require multidisciplinary teams, including people with expertise in areas not yet involved in the field of endocrine disruption, such as mathematical modellers. However, until such research is done, it will not be possible to decide how important an issue endocrine disruption is to wildlife, and how that importance compares to the other factors adversely affecting wildlife, such as habitat loss, climate change, and the introduction of exotic species and novel diseases.     

Inter-population variability in the reproductive morphology of the shore crab (Carcinus maenas): evidence of endocrine disruption in a marine crustacean?

Environmental contaminants that are capable of causing endocrine disrupting effects are currently a major cause for concern. These chemicals are known to influence the reproductive development of vertebrates by mimicking or antagonising the actions of endogenous hormones. However, little is known regarding their potential effects on invertebrates. Here we examine variations in the reproductive morphology of the shore crab (Carcinus maenas) for evidence of endocrine disruption. Crabs were collected from a number of sites comprising a putative gradient of exposure to endocrine disrupting chemicals. Patterns of inter-population variability in the expression of sexually dimorphic traits were then examined for evidence of hormone disruption. Extensive variability was detected and patterns of chelal morphology were consistent with the gradient of endocrine disruption. However, overall, the patterns of morphological variability were not consistent with hormonally-mediated effects. This suggests that shore crabs are not susceptible to the same type of endocrine disrupting effects that have been detected in vertebrates, which are most commonly mediated via the oestrogen receptor. However, the potential for androgenic effects on crustacean morphology are discussed.     

Developmental,Reproductive, and Demographic Alterations in Aquatic Wildlife: Establishing Causality between Exposure to Endocrine‐active Compounds (EACs) and Effects

This brief overview discusses the difficulty of demonstrating causal associations between exposure to endocrine active compounds (EACs) and the occurrence of developmental, reproductive, or demographic disturbances in aquatic wildlife. While for biological responses at the suborganism level correlational or causal evidence of an EAC etiology has been established in a number of cases, well proven examples of ecological consequences of endocrine disruption are rather few in number. The attribution of causality is complicated due to (i) lack of data on EAC exposure and bioaccumulation, (ii) lack of specific biomarkers and endpoints, together with insufficient knowledge on the mechanisms and conditions by which EAC‐induced disruption of endocrine functions translates into impaired organism development and reproduction, and (iii) insufficient understanding of the importance of species diversity in endocrine physiology and life histories for the consequences of endocrine disruption. Future research should address these gaps in our understanding of EAC exposure and effects, but additionally needs to pay more attention (i) to ecological determinants influencing the population‐level consequences of the endocrine disruption of developÍmental and reproductive functions, and (ii) to the use of epidemiological principles and approaches.     

Comparative study of 17 β-estradiol on endocrine disruption and biotransformation in fingerlings and juveniles of Japanese sea bass Lateolabrax japonicus

Estrogenic contaminants in the aquatic environment are associated with endocrine disruption and feminization in fish. The effects of endocrine disrupting chemicals (EDCs) on fish have been well documented. However, very few studies have focused on 17 β-estradiol (E2) and its effects on endocrine system and biotransformation in a single prolonged exposure. This study investigated changes in the levels of serotonin (5-hydroxytryptamine) and acetyl choline esterase (AchE) in brain, cortisol in plasma and Ethoxyresorufin-O-deethylase (EROD) activity in gill of two different size groups (fingerlings and juveniles) of Japanese sea bass (Lateolabrax japonicus) upon exposure to two sub-lethal concentrations (200 and 2000 ng L⁻¹) of E2 for 30 d. The results indicate that cortisol level and EROD activity significantly increased in both groups, whereas serotonin level increased in juveniles and decreased in fingerlings due to E2 exposure. The correlation analysis revealed that E2 significantly affected the endocrine and biotransformation systems in both age groups.     

环境激素氰戊菊酯和有机锡对轮虫生活史特征的影响

采用单"克隆"培养和群体培养的方法,研究了具有环境雌激素效应药物氰戊菊酯(Fenvalerate)和雌性雄性化激素效应药物三丁基氯化锡(TBTC)对萼花臂尾轮虫(Brachionus calyciflorus)生命周期中各发育阶段的历时以及种群增长的影响,结果表明,氰戊菊酯和TBTC对萼花臂尾轮虫的生长发育和种群增长有明显的效应,氰戊菊酯使生殖期延长(200和1000μg/L),生殖后期缩短,平均寿命也缩短(除1000μg/L),总产卵量和种群增长率升高;而经TBTC处理生殖前期延长(1和5μg/L),生殖期和生殖后期缩短,平均寿命也缩短,总产卵量和种群增长率较对照组也有下降,批次携卵量也受到两种药物的影响,且萼花臂尾轮虫的总产卵量随着氰戊菊酯和TBTc的浓度呈曲线相关,氰戊菊酯:Y=-0.6745X2+6.6884X+5.855(R2=0.7027);TBTC:Y=0.2054X2-2.3 178X+16.666(R2=0.6535),研究表明环境雌激素氰戊菊酯和雌性雄性化激素TBTC对萼花臂尾轮虫生活史特征影响表现出一定差异.     

Influence of a Xenobiotic Mixture (PCB and TBT) Compared to Single Substances on Swimming Behavior or Reproduction of Daphnia magna

Aroclor 1254, a technical PCB mixture (polychlorinated biphenyls) and TBT (tributyltinchloride) are environmental pollutants that cause a broad spectrum of acute toxic and chronic effects in aquatic animals. In this paper, the sensitivity of Daphnia magna to chronic exposure to mixed xenobiotics was evaluated under laboratory conditions. The results show that xenobiotic mixtures (50 % each of the single compounds) were more toxic than individual xenobiotics alone. By measuring behavioral parameters of animals, it becomes evident that exposure to single xenobiotics significantly affects daphnids: exposure led finally to a rapid decrease in mean swimming activity and also caused changes in preferred swimming depth, with daphnids preferring the upper layers of aquaria. The mixture altered the swimming behavior even more strongly compared to the group stressed by single chemicals. Finally, all daphnids sank to the bottom of the aquaria, still alive, but inactive at the end of the exposure period. In addition, we investigated the reproductive capacity (number of newborn per female and day). PCB did not affect the number of newborn significantly, TBT‐stress led to an evidently decreased number of young daphnids and the xenobiotic mixture decreased reproduction even more. In conclusion, we found significant effects of the single compounds as well as approximately additive (swimming behavior) and synergistic (reproduction) effects of the chemical mixture on daphnids indicating the possibility of dramatic ecological consequences of the occurrence of mixed xenobiotic substances in the aquatic environment.     

Evaluating legacy contaminants and emerging chemicals in marine environments using adverse outcome pathways and biological effects-directed analysis

Natural and synthetic chemicals are essential to our daily lives, food supplies, health care, industries and safe sanitation. At the same time protecting marine ecosystems and seafood resources from the adverse effects of chemical contaminants remains an important issue. Since the 1970s, monitoring of persistent, bioaccumulative and toxic (PBT) chemicals using analytical chemistry has provided important spatial and temporal trend data in three important contexts; relating to human health protection from seafood contamination, addressing threats to marine top predators and finally providing essential evidence to better protect the biodiversity of commercial and non-commercial marine species. A number of regional conventions have led to controls on certain PBT chemicals over several years (termed ‘legacy contaminants’; e.g. cadmium, lindane, polycyclic aromatic hydrocarbons [PAHs] and polychlorinated biphenyls [PCBs]). Analytical chemistry plays a key role in evaluating to what extent such regulatory steps have been effective in leading to reduced emissions of these legacy contaminants into marine environments. In parallel, the application of biomarkers (e.g. DNA adducts, CYP1A-EROD, vitellogenin) and bioassays integrated with analytical chemistry has strengthened the evidence base to support an ecosystem approach to manage marine pollution problems. In recent years, however, the increased sensitivity of analytical chemistry, toxicity alerts and wider environmental awareness has led to a focus on emerging chemical contaminants (defined as chemicals that have been detected in the environment, but which are currently not included in regulatory monitoring programmes and whose fate and biological impacts are poorly understood). It is also known that natural chemicals (e.g. algal biotoxins) may also pose a threat to marine species and seafood quality. Hence complex mixtures of legacy contaminants, emerging chemicals and natural biotoxins in marine ecosystems represent important scientific, economic and health challenges. In order to meet these challenges and pursue cost-effective scientific approaches that can provide evidence necessary to support policy needs (e.g. the European Marine Strategy Framework Directive), it is widely recognised that there is a need to (i) provide marine exposure assessments for priority contaminants using a range of validated models, passive samplers and biomarkers; (ii) integrate chemical monitoring data with biological effects data across spatial and temporal scales (including quality controls); and (iii) strengthen the evidence base to understand the relationship between exposure to complex chemical mixtures, biological and ecological impacts through integrated approaches and molecular data (e.g. genomics, proteomics and metabolomics). Additionally, we support the widely held view that (iv) that rather than increasing the analytical chemistry monitoring of large number of emerging contaminants, it will be important to target analytical chemistry towards key groups of chemicals of concern using effects-directed analysis. It is also important to evaluate to what extent existing biomarkers and bioassays can address various classes of emerging chemicals using the adverse outcome pathway (AOP) approach now being developed by the Organization for Economic Cooperation and Development (OECD) with respect to human toxicology and ecotoxicology.     

Endocrine disrupting compounds: can they target the immune system of fish?

Endocrine disruption, in particular disruption by estrogen-active compounds, has been identified as an important ecotoxicological hazard in the aquatic environment. Research on the impact of endocrine disrupting compounds (EDCs) on wildlife has focused on disturbances of the reproductive system. However, there is increasing evidence that EDCs affect a variety of physiological systems other than the reproductive system. Here, we discuss if EDCs may be able to affect the immune system of fish, as this would have direct implications for individual fitness and population growth. Evidence suggesting an immunomodulatory role of estrogens in fish comes from the following findings: (a) estrogen receptors are expressed in piscine immune organs, (b) immune gene expression is modulated by estrogen exposure, and (c) pathogen susceptibility of fish increases under estrogen exposure.     

A probabilistic approach to exposure risk assessment

The introduction of hazardous substances into the environment has long been recognized as being a cause of several diseases in humans, wildlife, and plants. The damaging character of suspected contaminants is usually assessed via a “reject/retain” design with no explicit link between levels of exposure and intensities of the potential adverse health effects even though this connection may be important for the development of public health regulations that limit exposure to hazardous substances. Here, we propose a probabilistic approach to exposure risk assessment as a way around this typical flaw. We develop a Bayesian model using proximity to the source of an alleged contaminant as a surrogate for exposure. Subsequently, we carry out an experimental study based on simulated data to illustrate the model implementation with real world data. We also discuss a possible way of extending the model to accommodate potential heterogeneity in the spatial distribution of the focal disease.     

Toxic chemicals in Canadian fish-eating birds

Cross-country comparison of DDE and PCB residue levels in cormorant, gull and tern eggs in Canada reveal that bird populations at the Great Lakes are most contaminated with those pollutants. DDE levels have been correlated with reproductive failure in Double-crested Cormorants in the Great Lakes with eggshell thinning as a major factor. Low reproductive success in Herring Gull colonies at Lake Ontario is associated with high chlorinated hydrocarbon levels in eggs. Fish-eating birds in the Wabigoon River system, northwestern Ontario, are among the most known mercury contaminated birds. It is suggested that the effects of mercury on the reproduction of fish-eating birds should be further examined there.Fish-eating birds occupy the highest levels of the food web and magnification of toxic chemicals through prey organisms in this web makes those birds vulnerable to the effects of environmental contaminants. Since fish-eating birds are present everywhere in Canada's freshwater and marine habitats and occupy various niches there, they may serve as pollution indicators in various food chains of our aquatic environment. Colonial birds are especially valuable indicators as pollution effects on total bird populations can be studied. Baseline information on fish-eating bird populations should now be collected everywhere in Canada for measuring present and future effects of environmental pollutants, as well as other man-made disturbances on their populations.     

Fate and effects of polydimethylsiloxane (PDMS) in marine environments

Polydimethylsiloxanes (PDMS) defoamers are used to improve process efficiency under extreme conditions during gas-oil separation, when other chemicals fail to perform. They are also used to reduce the oil content of process waters discharged to the marine environment, thereby serving an important function in reducing oil pollution. As a consequence of these applications small quantities of PDMS may also be released into the environment. This paper reviews the fate of PDMS in the marine environment and the extensive effect studies that have been conducted. These demonstrate the absence of adverse effects on a wide range of marine species.     

Review on toxicity testing with marine macroalgae and the need for method standardization--exemplified with copper and phenol

Toxic effects on macroalgae have been compiled. Eighty-two articles have been found in literature during 1959-2000. A total of 120 substances were investigated using 65 different macroalgae species. About one-third of the tested compounds were organic substances (33%), another third metal-organic substances (35%), and the last third were oils (14%), metals (8%), detergents (7.5%) and other inorganic chemicals (2.5%). Half of the substances were only tested once on a single species. Likewise, toxicity data has only been reported for one chemical tested on a single occasion for about half of the 65 species. Thus little is known about the toxic effects on marine macroalgae. The objectives of the previous studies undertaken varied and therefore the toxicity data was presented in numerous ways, e.g. using different exposure times, temperature, light intensity, light regime, salinity, and nutrients, which makes a direct comparison of the data difficult. This review also shows that many stages in the lifecycle of macroalgae are often more sensitive to toxic substances than other aquatic organisms. Consequently, tests using macroalgae may discover toxicity earlier, which would in turn also protect the fauna. If toxic compounds have a negative affect on the distribution and growth of structurally and functionally dominating macroalgae, there may indirectly be a large and harmful influence on the whole marine coastal ecosystem. For this reason tests on macroalgae should be included in control programs along the coasts.     

Gonadal histology and serum vitellogenin levels of bigeye tuna Thunnus obesus from the Northern Pacific Ocean--absence of endocrine disruption bio-indicators

Endocrine disrupting chemicals such as organochlorines have been detected in a large number of marine fish. Histological observation of the gonads, measurement of serum vitellogenin (VTG) level and of liver polychlorinated biphenyl (PCB) content were performed to evaluate the reproductive health and the contamination with endocrine disruptors in bigeye tuna Thunnus obesus, collected in the northern Pacific Ocean in 1999 and 2000. Abnormalities commonly found in species affected by endocrine disruptors such as the presence of oocytes in the testis or elevated serum VTG levels were not found in any of males examined. Both males and females had only small amounts of liver PCB content. The results suggest that currently there is little if any risk of organochlorine contamination or endocrine disruption of gonadal function in bigeye tuna from the northern Pacific Ocean. However, further studies are necessary to evaluate the health status of the open sea fishery resources.     

Concentration and distribution of hydrophobic organic contaminants and metals in the estuaries of Ukraine

In this study of Ukrainian estuaries, sediments and tissues from the Dnieper and Boh estuaries and Danube Delta on the mainland, Sevastopol and Balaklava Bays on the Crimean Peninsula, and coastal Black Sea along the Crimean Peninsula were collected in 2006. Contaminant analyses included several metals, the hydrophobic organic chemicals (HOCs) polychlorinated biphenyls, several chlorinated pesticides, and polycyclic aromatic hydrocarbons. When compared to estuarine sediments globally, the Ukrainian sediments were found to be moderately contaminated. However, several metals, especially mercury, were often shown to be elevated in the tissues of the Ukrainian organisms in comparison to organisms from other estuarine locations. Sediment quality guidelines indicate some of the estuarine sediments could be sufficiently contaminated to cause adverse toxicological effects. This investigation represents the first extensive study of HOC and metal baseline concentrations and distributions in Ukrainian estuaries and seeks to characterize exposures to aquatic organisms living in these systems.     

基于多指标综合评分法筛选地表水环境优先污染物——以湖北涨渡湖为例

人类活动和社会经济迅速发展导致大量化学品排放进入地表水环境,对水生生态系统和人类健康产生诸多不利影响,如何从众多的化学品中筛选识别出具有潜在危害的优先污染物是水污染治理和管控的关键.本研究基于污染物环境暴露水平、持久性、生物累积性、生态风险和人体健康风险5个评价参数,构建多指标综合评分法定量筛选识别地表水环境优先污染物类别,并应用于涨渡湖水体中优先污染物清单的建立.污染物环境暴露水平基于靶向分析综合考虑了污染物环境实测浓度和检出频率.目标污染物持久性和生物累积性毒害性参数分别采用生物降解系数和正辛醇-水分配系数来表征.此外在物种敏感度分布法和评估因子法的基础上计算生态风险熵以定量表征生态风险,人体健康风险则由终生致癌风险指数或危害指数来表征.基于该多指标综合评分法可于涨渡湖水体7类151种特征污染物中筛查出41种优先污染物,主要包括11种多氯联苯、8种有机氯农药、6种多环芳烃、4种邻苯二甲酸酯、4种挥发性有机物和8种金属元素.鉴于不同地表水环境污染状况不同,通过多指标综合评分法可建立因地制宜的优先污染物清单,从而有利于形成以保护水生生物和人类健康为最终目标的优先污染物水质基准,为地表水环境污染物管控及治理提供方法学支撑和科学依据.     

Reduction in the testosterone levels by PCBs and DDE in Dall''s porpoises of northwestern North Pacific

The increasing residue levels of PCBs and DDE in the blubber of dalli-type Dall's porpoises were found to have a negative effect on the testosterone levels in blood. Decrease in the levels of testosterone was statistically significant with increase in DDE concentrations. The results obtained suggest that the present levels of environmental contamination by persistent organochlorines can cause an imbalance of sex hormones and subsequent reproductive abnormalities in wild. The other hormone measured, aldosterone, which has no sexual function, was independent of the effects of both PCBs and DDE.     

Eutrophication, Water Borne Pathogens and Xenobiotic Compounds: Environmental Risks and Challenges

Recent advances in pollution control and monitoring technologies, improved analytical capability, changes in government priorities and results of scientific studies have substantially changed our views and perceptions towards marine pollution in the last two decades. Globally, the problems caused by eutrophication, water borne pathogens and xenobiotic compounds are likely to be exacerbated and pose significant ecological and/or public health risks in the coming years, especially in developing countries. The large amount of anthropogenic input of nutrients has caused major changes in the structure and function of phytoplankton, zooplankton, benthic and fish communities over large areas, and such a trend is likely to continue in many coastal waters. Escalated public health risks associated with the increases in frequency and severity of toxic algal blooms are also of growing concern. Reduction of nutrient input through changes in land-use and farming practises, and the development of cost-effective methods for nutrient removal are required. Water borne pathogens affect large numbers of people through consumption of contaminated seafood and direct contact with contaminated water, and such problems are much more serious in developing countries. Current techniques in monitoring bacterial indicators in water and shellfish have clear limitations and cannot afford adequate protection to safeguard public health. Emerging molecular techniques, such as multiplex PCR and specific gene probes, are likely to provide new and cost effective tools for monitoring water borne pathogens in the coming years. Nowadays, xenobiotic compounds can be found almost everywhere in any marine ecosystems. Although these compounds normally occur at very low concentrations and their effects are not well understood, there is growing concern about the chronic exposure and bioconcentration/biomagnification of xenobiotic compounds. In particular, endocrine disrupters which may cause reproductive dysfunction and threaten species survival, are of growing concern. At present, most of our knowledge on toxic effects of xenobiotic compounds is derived from short-term exposure of a single species to high (environmentally unrealistic) and uniform concentrations under laboratory conditions. Data so derived are largely inadequate in predicting ecological effects in the field, in which multi-species are being exposed to varying, low concentrations under an interacting and complex environment. NOEC and LOEC for population/community/ecosystem, as well as the time required for population/community/ecosystems to recover after toxicant insult, are poorly known. These important topics will become the major endeavours for ecotoxicologists in the years to come.