The immunotoxicity of environmental contaminants to marine wildlife: A review

Virus-associated mass mortalities among several marine mammal populations inhabiting industrialized coastal areas have generated an interest in wildlife immunotoxicology. Despite the isolation of previously uncharacterized viruses from victims, a contribution of immunotoxic contaminants to the severity of the outbreaks could not be ruled out. Fish-eating marine mammals, including seals, occupy high trophic levels in the aquatic food chain, and accumulate high levels of contaminants including polychlorinated biphenyls (PCBs), polychlorinated dibenzo-p-dioxins (PCDDs), and polychorinated dibenzofurans (PCDFs). Such chemicals have been found to be immunotoxic at low doses in studies of laboratory animals. While associations have been established between environmental contaminants and various adverse biological effects in certain free-ranging seal populations, evidence for immunotoxicity has, until recently, been lacking. To this end, we carried out an immunotoxicological study, in which captive harbor seals were fed herring from either relatively uncontaminated sites of the Atlantic Ocean, or from the highly contaminated Baltic Sea. In this review, we summarize the contaminant-related immunosuppression observed in the captive group of seals fed herring from the Baltic Sea, and discuss these results in the context of what is currently known about outbreaks of virus infection, comparative immunology, and environmental contaminants. We also describe two parallel studies, in which laboratory rats exposed as adults or perinatally to the contaminants in the Baltic Sea herring, exhibited immunotoxicity. On the basis of these and other studies, we conclude that complex mixtures of environmental contaminants may represent a real immunotoxic risk to free-ranging marine mammals in many areas of Europe and North America.     

The Role of Immunotoxic Environmental Contaminants in Facilitating the Emergence of Infectious Diseases in Marine Mammals

A series of high profile outbreaks of newly described diseases in humans, domestic animals and wildlife has attracted widespread interest in the topic of Emerging Infectious Diseases (EIDs). Marine mammals are no exception: since 1987 several mass mortalities have been observed following infection with viruses previously undescribed in the populations or species in question. As with terrestrial examples, some of these outbreaks have followed either migrations associated with large-scale ecological changes or the introduction of virus from domestic animals. However, marine mammals warrant special concern in the context of emerging infectious diseases: they typically occupy high trophic levels and can therefore be highly contaminated with immunotoxic chemicals. Persistent Organic Pollutants (POPs), including polychlorinated -biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), -dibenzofurans (PCDFs) and related compounds, are demonstrated immunotoxicants in laboratory animals, as well as marine mammals. Immunotoxic contaminants may represent a factor that facilitates disease emergence, and may lead to the creation of susceptible “reservoirs” for new pathogens in contaminated marine mammal populations. The factors underlying the emergence and exchange of pathogens among marine mammals, domestic animals, and humans demand multidisciplinary study and invite regulatory and conservation scrutiny. The complexity of this issue may be best addressed through an integrated human and ecological risk assessment framework.     

Comparison of Mercury Contamination in Live and Dead Dolphins from a Newly Described Species,Tursiops australis

Globally it is estimated that up to 37% of all marine mammals are at a risk of extinction, due in particular to human impacts, including coastal pollution. Dolphins are known to be at risk from anthropogenic contaminants due to their longevity and high trophic position. While it is known that beach-cast animals are often high in contaminants, it has not been possible to determine whether levels may also be high in live animals from the same populations. In this paper we quantitatively assess mercury contamination in the two main populations of a newly described dolphin species from south eastern Australia, Tursiops australis. This species appear to be limited to coastal waters in close proximity to a major urban centre, and as such is likely to be vulnerable to anthropogenic pollution. For the first time, we were able to compare blubber mercury concentrations from biopsy samples of live individuals and necropsies of beach-cast animals and show that beach-cast animals were highly contaminated with mercury, at almost three times the levels found in live animals. Levels in live animals were also high, and are attributable to chronic low dose exposure to mercury from the dolphin''s diet. Measurable levels of mercury were found in a number of important prey fish species. This illustrates the potential for low dose toxins in the environment to pass through marine food webs and potentially contribute to marine mammal deaths. This study demonstrates the potential use of blubber from biopsy samples to make inferences about the health of dolphins exposed to mercury.     

Review of stress in marine mammals

There has been a growing concern over the last few decades about theeffects of environmental stress, including anthropogenic impacts, onmarine mammals. This paper provides an overview of the wide range ofanthropogenic stressors that marine mammals may encounter and the levelof understanding on their potential effects. Sources of stress andphysiological responses of the animals are explored. Many of the lifehistory traits of marine mammals (i.e., long-life spans, late maturity,relatively low reproductive potential, and feeding high in the foodchain), make them susceptible to various anthropogenic stressors. Sincemarine mammals are exposed to a diverse array of multiple stressors,this paper focuses on three case studies (acute and chronic effects fromoil spills; chronic effects from environmental contaminants, andfishery-induced stress) to emphasize potential relevant hazards and toprovide a perspective on the use of marine mammals in assessingecosystem health. Additional research to enhance our understanding ofstress on marine mammals and to provide the science needed to guidemanagement decisions is recommended.     

海洋微塑料污染的生态效应研究进展

海洋微塑料污染已成为全球性环境问题。微塑料粒径小,易与海洋生物发生相互作用,可通过多种途径进入海洋生物体内,并在其组织和器官中蓄积和转移,对机体产生毒害。微塑料可沿食物链进行传递,威胁海洋生态系统的健康与稳定。因此,海洋生物与微塑料的相互作用以及海洋微塑料污染的生态效应成为当前研究的热点。综述微塑料的生物附着、生物摄入、对海洋生物的毒性效应及其与化学污染物的复合毒性效应研究的基础上,提出未来微塑料生态效应研究应重点关注我国海洋环境中微塑料的污染现状及生物摄入状况、微塑料的生物效应及其毒理学机制研究、微塑料与其他污染物的复合效应、以及微塑料在海洋生态系统中的作用及其生物地球化学行为等。     

Pollution effects on fisheries — potential management activities

Management of ocean pollution must be based on the best available scientific information, with adequate consideration of economic, social, and political realities. Unfortunately, the best available scientific information about pollution effects on fisheries is often fragmentary, and often conjectural; therefore a primary concern of management should be a critical review and assessment of available factual information about effects of pollutants on fish and shellfish stocks. A major problem in any such review and assessment is the separation of pollutant effects from the effects of all the other environmental factors that influence survival and well-being of marine animals. Data from long-term monitoring of resource abundance, and from monitoring of all determinant environmental variables, will be required for analyses that lead to resolution of the problem. Information must also be acquired about fluxes of contaminants through resource-related ecosystems, and about contaminant effects on resource species as demonstrated in field and laboratory experiments. Other possible management activities include: (1) encouragement of continued efforts to document clearly the localized and general effects of pollution on living resources; (2) continued pressure to identify and use reliable biological indicators of environmental degradation (indicators of choice at present are: unusually high levels of genetic and other anomalies in the earliest life history stages; presence of pollution-associated disease signs, particularly fin erosion and ulcers, in fish; and biochemical/physiological changes); and (3) major efforts to reduce inputs of pollutants clearly demonstrated to be harmful to living resources, from point sources as well as ocean dumping. Such pollution management activities, based on continuous efforts in stock assessment, environmental assessment, and experimental studies, can help to insure that rational decisions will be made about uses and abuses of coastal/estuarine waters.     

Genotoxic, carcinogenic, and teratogenic hazards in the marine environment, with special reference to the Mediterranean Sea.

Genotoxic, carcinogenic, and teratogenic hazards arising out of pollution in the marine environment are discussed in this article, with special reference to the situation in the Mediterranean area. A number of chemical compounds or complex mixtures relevant to marine pollution, either natural or of anthropogenic origin, are tentatively listed, along with protective factors which may play a counteracting role in the same environment. Harmful substances tend to undergo interactions and transformations in seawater, sediments, and marine biota, due to physical, chemical, microbial, or light-mediated mechanisms. Bioaccumulation phenomena in marine organisms may result from food-chain biomagnification processes or from concentration of pollutants by filter feeders. A variety of sources can account for marine pollution by genotoxic, carcinogenic, and teratogenic compounds, but there is a relative paucity of analytical data concerning the Mediterranean. Metabolic transformations of xenobiotics occur in all marine organisms, the biochemical mechanisms in fish being comparable to those which have been extensively investigated in mammals. Induction of metabolic pathways, and especially of the mixed-function oxygenase system, represents the earliest warning signal of exposure to pollutants. Occurrence of neoplastic diseases is documented by experimental and field studies in marine vertebrates as well as in invertebrates. The association with local pollution phenomena has been recognized in several studies, but other etiopathogenetic factors may be also involved, and in some cases tumors have been reported to be unrelated to chemical pollution. Genotoxic agents have been detected by means of suitable techniques in seawater, sediments, and marine organisms. Several studies have investigated the presence of carcinogen-DNA adducts, DNA damage and repair processes, and cytogenetic alterations, such as chromosomal aberrations, sister-chromatid exchanges, and micronuclei, in tissues of marine organisms. However, monitoring of these end-points under field conditions encounters some limitations and problems. Even more fragmentary is the information on teratogenic effects in marine organisms, although interesting test systems have been set up. On the whole, a quite extensive database on all these toxicological issues is already available in the literature, but further studies are warranted for an adequate assessment of genotoxic, carcinogenic, and teratogenic hazards, and possibly counteracting factors in the marine environment, and specifically in the Mediterranean Sea.     

Selection of reference genes for quantitative RT-PCR studies in striped dolphin (Stenella coeruleoalba) skin biopsies

Background  

Odontocete cetaceans occupy the top position of the marine food-web and are particularly sensitive to the bioaccumulation of lipophilic contaminants. The effects of environmental pollution on these species are highly debated and various ecotoxicological studies have addressed the impact of xenobiotic compounds on marine mammals, raising conservational concerns. Despite its sensitivity, quantitative real-time PCR (qRT-PCR) has never been used to quantify gene induction caused by exposure of cetaceans to contaminants. A limitation for the application of qRT-PCR is the need for appropriate reference genes which allow the correct quantification of gene expression. A systematic evaluation of potential reference genes in cetacean skin biopsies is presented, in order to validate future qRT-PCR studies aiming at using the expression of selected genes as non-lethal biomarkers.     

Compositional Discrimination of Decompression and Decomposition Gas Bubbles in Bycaught Seals and Dolphins

Gas bubbles in marine mammals entangled and drowned in gillnets have been previously described by computed tomography, gross examination and histopathology. The absence of bacteria or autolytic changes in the tissues of those animals suggested that the gas was produced peri- or post-mortem by a fast decompression, probably by quickly hauling animals entangled in the net at depth to the surface. Gas composition analysis and gas scoring are two new diagnostic tools available to distinguish gas embolisms from putrefaction gases. With this goal, these methods have been successfully applied to pathological studies of marine mammals. In this study, we characterized the flux and composition of the gas bubbles from bycaught marine mammals in anchored sink gillnets and bottom otter trawls. We compared these data with marine mammals stranded on Cape Cod, MA, USA. Fresh animals or with moderate decomposition (decomposition scores of 2 and 3) were prioritized. Results showed that bycaught animals presented with significantly higher gas scores than stranded animals. Gas composition analyses indicate that gas was formed by decompression, confirming the decompression hypothesis.     

Monitoring population‐level responses of marine mammals to human activities

We provide guidance for monitoring whether human activities affect the physiology or behavior of marine mammals and, if so, whether those effects may lead to changes in survival and reproduction at the population level. We suggest that four elements be included in designing and implementing such a monitoring program. The first is development of a theory of change: a set of mechanistic hypotheses that outline why a given activity might be expected to have one or more measurable effects on individuals and populations, and ideally the magnitude, timing, and duration of the effects. The second element, definition of biologically meaningful effect sizes, ultimately facilitates the development of a monitoring program that can detect those magnitudes of effect with the desired levels of precision. The third element, selection of response variables for monitoring, allows inference to whether observed changes in the status of individuals or populations are attributable to a given activity. Visual observations, passive acoustic and tagging instruments, and direct physical measurements all can provide data that facilitate quantitative hypothesis testing. The fourth element is specification of the temporal sequence of monitoring. These elements also can be used to inform monitoring of the responses of other taxonomic groups to human activities.     

Stress physiology in marine mammals: how well do they fit the terrestrial model?

Stressors are commonly accepted as the causal factors, either internal or external, that evoke physiological responses to mediate the impact of the stressor. The majority of research on the physiological stress response, and costs incurred to an animal, has focused on terrestrial species. This review presents current knowledge on the physiology of the stress response in a lesser studied group of mammals, the marine mammals. Marine mammals are an artificial or pseudo grouping from a taxonomical perspective, as this group represents several distinct and diverse orders of mammals. However, they all are fully or semi-aquatic animals and have experienced selective pressures that have shaped their physiology in a manner that differs from terrestrial relatives. What these differences are and how they relate to the stress response is an efflorescent topic of study. The identification of the many facets of the stress response is critical to marine mammal management and conservation efforts. Anthropogenic stressors in marine ecosystems, including ocean noise, pollution, and fisheries interactions, are increasing and the dramatic responses of some marine mammals to these stressors have elevated concerns over the impact of human-related activities on a diverse group of animals that are difficult to monitor. This review covers the physiology of the stress response in marine mammals and places it in context of what is known from research on terrestrial mammals, particularly with respect to mediator activity that diverges from generalized terrestrial models. Challenges in conducting research on stress physiology in marine mammals are discussed and ways to overcome these challenges in the future are suggested.     

CYTOCHROME P450 1A1 EXPRESSION IN CETACEAN INTEGUMENT: IMPLICATIONS FOR DETECTING CONTAMINANT EXPOSURE AND EFFECTS

Contaminant related health risks to marine mammals are typically inferred from the levels of contaminants measured in blubber. Such measurements alone are insufficient to indicate the likelihood of biological effects from contaminant exposure, especially for contaminants that do not bioaccumulate. Cytochrome P450 1A1 (CYP1A1) in mammals is induced by, and involved in, the metabolism of planar halogenated aromatic hydrocarbons and polycyclic aromatic hydrocarbons, chemicals of concern in aquatic systems. CYP1A induction is a molecular response to exposure to these inducers in many vertebrates. Using immunohistochemistry, we semiquantitatively measured CYP1A1 expression in integument (epidermis and blubber) collected by biopsy or at necropsy from 17 species of cetaceans. CYP1A1 expression was detected in all species and, in some cases, varied both within and between species. CYP1A1 expression in mysticetes was comparable to that in odontocetes. Assessing how the differences in contaminant burdens, life history parameters, and physiological condition between individuals, populations, or species affect CYP1A1 expression in cetacean integument is essential to the interpretation of this induction as a biomarker of exposure to and effects of contaminants. Detection of CYP1A1 expression in integument samples offers a relatively simple, non-lethal technique to study biological changes associated with contaminant exposure in cetaceans.     

Epidermal diseases in bottlenose dolphins: impacts of natural and anthropogenic factors.

Experimental studies have highlighted the potential influence of contaminants on marine mammal immune function and anthropogenic contaminants are commonly believed to influence the development of diseases observed in the wild. However, estimates of the impact of contaminants on wild populations are constrained by uncertainty over natural variation in disease patterns under different environmental conditions. We used photographic techniques to compare levels of epidermal disease in ten coastal populations of bottlenose dolphins (Tursiops truncatus) exposed to a wide range of natural and anthropogenic conditions. Epidermal lesions were common in all populations (affecting > 60% of individuals), but both the prevalence and severity of 15 lesion categories varied between populations. No relationships were found between epidermal disease and contaminant levels across the four populations for which toxicological data were available. In contrast, there were highly significant linear relationships with oceanographic variables. In particular, populations from areas of low water temperature and low salinity exhibited higher lesion prevalence and severity. Such conditions may impact on epidermal integrity or produce more general physiological stress, potentially making animals more vulnerable to natural infections or anthropogenic factors. These results show that variations in natural environmental factors must be accounted for when investigating the importance of anthropogenic impacts on disease in wild marine mammals.     

土壤生物与土壤污染研究前沿与展望

随着社会经济发展,人类生产活动对自然环境产生越来越广泛深刻的影响,土壤污染已成为危及生态系统稳定、农产品质量安全和人体健康的突出环境问题之一。重金属、有机污染化合物、病原菌及抗性基因等各类污染物大量进入土壤后,对土壤生物系统造成毒害作用,影响到土壤生态功能;另一方面,土壤生物如细菌、真菌、土壤动物等在一定程度上能够适应土壤污染,深刻影响着污染物在土壤中的迁移转化过程,在土壤污染修复中具有潜在重要作用。从土壤污染的生态毒理效应、土壤生物对土壤污染的响应与适应机制、污染土壤修复原理与技术等三方面综述了土壤生物与土壤污染相关研究前沿,展望了重点研究方向。     

USING ORGANOCHLORINE POLLUTANTS TO DISCRIMINATE MARINE MAMMAL POPULATIONS: A REVIEW AND CRITIQUE OF THE METHODS1

Organochlorine pollutants are potentially useful for identifying discrete populations of marine mammals that overlap in geographic distribution. However, many factors unrelated to geographical distribution may affect the chemical burden of individual animals or of entire population components even within a homogeneously distributed population. These factors include. among others, nutritional state, sex, age, trophic level, distance of habitat from mainland and pollution source, excretion. metabolism, and tissue composition. Sample storage and analytical methodology may also be an important source of variation. These, and any other factors, must be identified and their effect ascertained before attempting any comparison between populations. This paper critically examines the nature and magnitude of the effects of these factors on organochlorine tissue loads in marine mammals. Pollutant concentrations can be strongly biased if carefully designed sampling regimes are not followed, but they are affected only moderately by sample treatment after collection. Conversely, ratios between concentrations of compounds, such as the DDE/tDDT or the tDDT/PCB ratios, seem less dependent on sampling regime but more affected by storage. analytical procedures and ecological variations such as distance from pollutant source or trophic level. Taking these effects into account, advice is provided about sampling and strategies for selection of variables that will improve the reliability of the comparisons between populations.     

Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community‐level responses

Biological communities are shaped by complex interactions between organisms and their environment as well as interactions with other species. Humans are rapidly changing the marine environment through increasing greenhouse gas emissions, resulting in ocean warming and acidification. The first response by animals to environmental change is predominantly through modification of their behaviour, which in turn affects species interactions and ecological processes. Yet, many climate change studies ignore animal behaviour. Furthermore, our current knowledge of how global change alters animal behaviour is mostly restricted to single species, life phases and stressors, leading to an incomplete view of how coinciding climate stressors can affect the ecological interactions that structure biological communities. Here, we first review studies on the effects of warming and acidification on the behaviour of marine animals. We demonstrate how pervasive the effects of global change are on a wide range of critical behaviours that determine the persistence of species and their success in ecological communities. We then evaluate several approaches to studying the ecological effects of warming and acidification, and identify knowledge gaps that need to be filled, to better understand how global change will affect marine populations and communities through altered animal behaviours. Our review provides a synthesis of the far‐reaching consequences that behavioural changes could have for marine ecosystems in a rapidly changing environment. Without considering the pervasive effects of climate change on animal behaviour we will limit our ability to forecast the impacts of ocean change and provide insights that can aid management strategies.     

Effects of zinc on microalgal biofilms in intertidal and subtidal habitats

Microalgal biofilms are sensitive to environmental conditions. Impacts of contaminants on assemblages of marine biofilm are often investigated in laboratories or in mesocosms. Such experiments are rarely representative of the effects of contaminants on biofilms under natural conditions. Studies in field situations, with enough power to detect impacts, are necessary to develop a better understanding of the effects of contaminants on ecological processes. Metals are a common contaminant of marine systems and can cause disturbances to assemblages. Using a new technique to experimentally deliver contaminants to microalgal assemblages, hypotheses were tested regarding the effects of zinc on microalgal biofilms growing on settlement panels in subtidal and intertidal habitats. PAM fluorometry was used to assess the amount and physiological state of biofilms on panels. Control panels deployed for 1 month in each habitat had significantly greater amounts of biofilm than those exposed to zinc. After deployment for 3 months, the results varied with location. The observed effects on the biofilm did not, however, cause significant changes in the macro-invertebrate assemblages that developed on the panels.     

Effects of some trace elements on the blood of Kuwait mullets, Liza Macrolepis (Smith)

Haemopathological changes attributed to heavy metal poisoning were observed in blood smears of Liza macrolepis (Smith) taken after exposures of 96 h to graded doses (mg/l) of copper (0.11–1.80), lead (1.15–18.36), and mercury (0.04–0.59), in a flow-through marin bioassay system. In general, changes in leucocytic profile appear to be correlated with pathological changes caused by increasing copper and mercury concentrations. By contrast, blood samples of mullets exposed to lead, showed significant polychromasia and + anisocytosis regardless of concentrations. The RBC count, haemoglobin content, and haemotocrit percentages were less valuable in diagnosis of copper and mercury effects.These manifestations of poisoning by trace elements bear a resemblance to the pathological changes that have been shown clinically and experimentally in mammals. Consequently, blood measurements on marine organisms may be diagnostic of undeirably high levels of copper and mercury, and so may constitute useful indicators of marine pollution.