Cells and Tissues

Toxicant-induced changes in cells and tissues are useful biomarkers. Some changes reflect a cell's failure to remain viable in the presence of toxicants and others reflect partially successful attempts to maintain homeostasis. For example, histological examination of the liver from an exposed organism might reveal many dead (necrotic) cells. In the same tissues, inflammation might be occurring in an attempt to isolate, remove, and replace damaged cells. Both necrosis and inflammation are common biomarkers. Other changes such as the cellular accumulation of damaged biomolecules or cells modified to cope with toxicant damage are also good histological biomarkers.

Cancer is a cellular response to carcinogen exposure that is carefully studied by ecotoxicologists. Several ecological studies have demonstrated the role of environmental toxicants on cancer etiology. For example, Puget Sound English sole (Parophrys vetulus) taken from sites with elevated sediment contamination showed high prevalence of liver cancers. Another case of elevated cancer prevalence (27% of dead adults) involved beluga whales (Delpinapterus leucas) inhabiting a contaminated reach of the St. Lawrence estuary.

Exposure studies at this level focus on the routes of contaminant movement into and out of cells, and differences in accumulation in various tissues. Generally, contaminant movement into and out of cells involves (1) simple diffusion across the membrane lipid bilayer or through an ion channel, (2) facilitated diffusion involving a carrier protein, (3) active transport, or (4) endocytosis. Some of these routes are designed for other purposes such as ATPase active transport of cations but facilitate movement of contaminants such as cadmium. Other mechanisms are more specific. For example, the multi-xenobiotic resistance (MXR) mechanism specifically removes moderately hydrophobic, planar contaminants from the cell.

Organ and Organ Systems

Toxicant effect on organs and organ systems is another major theme in classical toxicology that also has a role in ecotoxicology. Organs can be targets of toxicant effects as in the case of the liver cancer mentioned above or can be routes of toxicant entry into the body as in the case of the integument, breathing organs, and digestive tract.

Contaminant effects on organs and organ systems are diverse. Pyrethoid pesticides modify essential ion exchange across amphibian skin. Fish gills are changed by exposure to low pH or high metal concentrations in such a way that normal ion and gas exchange are altered. Some contaminants (teratogens) can cause abnormal organ development. For example, fish embryos develop cardiovascular abnormalities if exposed to high concentrations of PAH. Still other toxicants compromise immunological competency, increasing susceptibility to infection or infestation. These examples represent only a few of the possible organ or organ system effects of contaminants on nonhuman species.

An issue attracting considerable attention at the moment is the ability of some environmental contaminants to modify endocrine functions such as those essential for sexual development and viability, or optimal metabolic activity. For example, the presence of the anti-fouling paint constituent, tributyltin, caused pervasive imposex (imposition of male features such as a penis or vas deferens on females) in whelk populations along the English and Northeast Pacific coasts. Contaminants that act as estrogen include DDT and its replacement, meth-oxychlor, nonylphenol from surfactant and detergent synthesis, and synthetic hormones from birth control pills that enter waterways from sewage treatment plants. Still other endocrine modifiers such as ammonium per-chlorate from military munitions disrupt thyroid function.

Exposure studies at this level ofbiological organization emphasize target organs. Some organs or organ systems are more prone to toxicant impacts due to their intimate contact with environmental media, location relative to blood circulation, or specific function. For example, the gills of aquatic organisms are often target organs for dissolved contaminants because of their intimate contact with the surrounding water. The liver or analogous organs in invertebrates are often sites of harmful effects because of their prominent detoxification function, that is, the liver cancer noted above in English sole was caused by contaminant activation during phase I reactions in the liver.

Whole Organism

Effects to individuals are used to make inferences about contaminant impacts on individual fitness, and indirectly, on populations and communities. The most commonly measured qualities are mortality, development, growth, reproduction, behavior, physiology, and bioenergetics.

Lethal effects are measured under different exposure scenarios. They might be measured during acute (4 days or shorter) or chronic (longer than 10% of an individual's lifespan) exposures. They might also be measured for contaminant exposure via different media such as water, air, food, and sediment. Most are studied in the laboratory in such a manner that physical, chemical, and biological factors influencing response to exposure are controlled. Therefore, mortality predicted for a particular exposure concentration might not completely define the mortality that would occur in the field where exposed individuals must successfully forage, compete with individuals of other species, avoid predators, and interact with individuals of the same species in order to remain alive.

Exposure studies that involve whole organisms emphasize bioaccumulation, the net accumulation of contaminant in an organism from water, air, or solid phases of its environment. Mathematical bioaccumulation models range from simple ones such as the one compartment model shown below to multicompartment, pharmacokinetic models:

ku k t Ct — CSource ~T [l — e e ] ke where Ct is the concentration in the organism at time, t, CSource is the concentration in the source, ku is uptake clearance, and ke is elimination rate constant. Most studies attempt to understand and quantify the influence of extrinsic (e.g., food type containing the contaminant) and intrinsic (e.g., animal sex or size) factors on bioaccumulation.

Population

Knowledge of effects to individuals is valuable, but insufficient, for predicting population-level impacts. Consequently, a growing number of ecotoxicologists study population-level effects directly. Such studies emphasize vital rates such as birth, death, stage change, or migration rates. Demographic models based on vital rates improve our ability to project consequences such as a drop in the population growth rate or increase in local population extinction risk.

Some population studies treat the population as one in which individuals are uniformly distributed in the area of interest but others consider the population (metapopulation) to be composed of subpopulations inhabiting habitat patches of different qualities, including different levels of contamination. The differences in vital rates, including exchange rates among patches, are used to project contaminant exposure consequences. With metapopulation models, effect manifestation at a distance from a contaminated patch can be explored: a population member can be exposed in one patch yet the effects might manifest in an uncontaminated patch after migration.

Community

Community ecotoxicology explores the consequences of contaminant exposure of and movement of contaminants within ecological communities. The majority of such studies are field studies either addressing scientific questions or applying knowledge to assess risk or define remediation action for a contaminated system. Like the biomarkers applied at lower levels of biological organization, bioindicators are applied by community ecotoxicologists. Bioindicators might be particularly sensitive species whose absence suggests an adverse impact. A community metric such as species richness, evenness, or diversity might also be used as an indicator of an adverse exposure consequence. Any study in which biological systems are applied to assess the structural and functional integrity of ecosystems is referred to as a biomonitoring study.

Smallmouth bass

White sucker

Redbreast sunfish

Snail

Periphyton

Figure 3 Mercury biomagnification in the South River (Waynesboro, Virginia, USA) illustrated with periphyton, a grazing snail (Leptoxis carinata), two intermediate fish species (redbreast sunfish, Lepomis auritus and white sucker, Catostomus commersoni), and a top predator species (smallmouth bass, Micropterus dolomieu). Author's unpublished data.

Exposure within communities is often explored in the context of contaminant trophic transfer. Depending on its properties, a contaminant can increase (biomagnify), decrease (trophic dilution), or not change in concentration with progression through a food web. Contaminants such as methylmercury or persistent organic pollutants (POPs) such as DDT biomagnify. Biomagnification can lead to adverse consequences to higher trophic level species such as the raptors and piscivorous birds mentioned above. Studies of food webs including omnivorous members require a measure of trophic status for species. A convenient measure of trophic status is provided by the nitrogen isotopic fractionation that occurs with each trophic exchange: the amount of heavy (15N) nitrogen increases in tissues relative to light ( N) nitrogen with each trophic exchange. The 6 15N is the conventional metric for expressing relative N isotopic abundances:

Graphs (e.g., Figure 3) or quantitative models of contaminant concentration in species within the subject community versus 6 15N facilitates prediction of contaminant movement in communities.

Ecosystems

Ecosystem-level studies vary widely in their spatial and temporal scales. Often ecosystem modeling techniques are applied to an easily definable ecosystem such as a contaminated lake or watershed. Fate and movement of

Worldwide

CO O

Preferential at polar latitudes

Preferential at mid-latitudes

Near source

3 Ring PAH 2-4 Cl PCB

2 Ring PAH

1 Cl PCB

4 Ring PAH 4-8 Cl PCB

log vapor pressure of subcooled liquid log octanol-air partition coefficient

Condensation temperature

Figure 4 Global movement of a POP is determined by several qualities including its (subcooled liquid) vapor pressure and condensation temperature which, together, determine its tendency to move into and remain in the atmosphere. A more volatile compound will be transported more by atmosphere movement than one that is less volatile. Its condensation temperature influences the latitudinal limits to which it might move. The octanol-air partition coefficient is also important because it reflects the POP's tendency to remain associated with the solid and liquid phases of the Earth versus the atmosphere. Here, polycyclic aromatic hydrocarbons (PAHs) with different numbers of aromatic rings and polychlorinated biphenyls (PCBs) with different numbers of chloride atoms are used to illustrate trends for global deposition of POP. This biospheric process is called global distillation.

contaminants are then modeled by computer or measured in extensive sampling programs. Larger-scale studies are required for contaminants amenable to wide spatial dispersion via atmospheric transport such as mercury from coal power plants or contaminants used widely by society such as atrazine, an herbicide applied in the North American Corn Belt. Often geographical information system (GIS) and remote sensing technologies are essential in these types of studies. In still other instances, a global perspective is required to adequately grasp the ecotoxicological consequences of contaminants. Current global issues are ozone depletion in the stratosphere due to chlorofluorcarbon (CFC) release, global warming due to greenhouse gas emissions, and global movement of persistent organic pollutants (Figure 4). More and more frequently, large-scale issues are emerging as critical ones in ecotoxicology.

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