A number of mechanisms have been proposed to describe the biomagnification process as it applies to persistent, hydrophobic organic compounds. The first model published to describe biomagnification of the insecticide DDT described the lipid co-assimilation mechanism. In this model, both lipids and contaminants are efficiently assimilated from food; however, a smaller fraction of lipids are retained as a result of metabolism of these nutrients to satisfy energetic requirements. Recalcitrant contaminants are retained in tissues and over time, in conjunction with the number of feeding events, magnify in concentration over that of ingested food. Under this mechanism, the maximum biomagnification potential in nondeterminant growing animals is inversely related to growth-conversion efficiency (i.e., rate of tissue growth relative to food consumption) when contaminant elimination from the animal approaches a value of 0. For determinant growers, biomagnification will continue to increase with age as a function of number of feeding events. In practice, most environmental contaminants do exhibit elimination, which will attenuate biomagnifica-tion in proportion to the magnitude of the elimination rate coefficient. In this case, the steady-state biomagnifi-cation factor will be positively related to the feeding rate of the animal and chemical assimilation efficiency from the diet and inversely proportional to the elimination rate coefficient and growth rate.
The lipid co-assimilation mechanism was also used to explain food web biomagnification. In this case, biomag-nification as achieved in top predator organisms is assumed to correspond to the inverse of ecological efficiency. Thus, the low energy transfer efficiency across trophic levels (<10%) coupled with efficient chemical transfer efficiencies and high chemical retention among different organisms results in progressively increased residues through successive trophic steps. This model indicates that the number of trophic levels and trophic transfer efficiencies across each step specify the maximum contamination achieved for top predators whereas growth and elimination by individual organisms attenuates food web biomagnification.
Although lipid co-assimilation as a mechanism of biomagnification is consistent with concepts of bioenergetics and trophodynamics, environmental chemists were quick to point out that such a mechanism is not consistent with chemical bioaccumulation through passive partitioning mechanisms as is thought to occur for hydrophobic organic chemicals. Lipids, fat-soluble vitamins, and hydrophobic organic contaminants cross biological membranes by passive diffusion. In the case of the proposed lipid co-assimilation model of biomagnification, net chemical diffusive flux would have to proceed in a direction of low concentration (ingested food and digesta of the gastrointestinal (GI) tract) to high concentration (animal tissues). The GI magnification model was subsequently developed as a competing model with lipid co-assimilation. This model is able to account for biomagnification while preserving chemical diffusion as the major mechanism of chemical flux between the organism and its gut contents.
Gastrointestinal magnification was first described in 1988. The model considers the GI tract and its contents as a separate compartment from animal tissues. The premise of the GI magnification model is that nutrient and lipid absorption occur independent of contaminants in the GI tract. The absorption of nutrients from digesta decreases both the volume and partitioning capacity of gut contents as digestion proceeds along the length of the intestines. The failure of mass balance within the GI tract compartment and loss of partitioning capacity raises the chemical potential of digesta in the GI tract above that of ingested food, providing the necessary gradient on which net diffusion can proceed from GI tract to animal even if the animal has a higher chemical potential than the food it has ingested. The animal thus equilibrates with the elevated chemical potential of its GI contents rather than its food.
Under the GI magnification model, the change in chemical partitioning capacity of feces relative to food and the volume reduction of feces produced relative to food consumed (i.e., diet absorption efficiency) provides the upper limit for the maximum biomagnification potential that can be achieved in an animal. These limits may vary according to the diet absorption efficiency for a given diet type and/or differences in digestive physiology between different species feeding on similar diets. The GI magnification model has been subject to experimental and field validation through studies that demonstrated increases in chemical potential of animal GI contents above that of ingested food. Careful laboratory measurements indicate maximum biomagnification potentials on the order of 3-12 in fish which appear to be consistent with field biomagnification factors experienced by fish. The GI magnification model has subsequently been adopted in numerous food web bioaccumulation models applied to hydrophobic organic contaminants. Food web bioaccumulation models allow consideration of relative exposures and biomagnification potentials in animals exposed to multiple diet items as defined by the diet matrix established for each species being modeled.
Recent studies have suggested amendments to the GI magnification model to account for additional physiological factors which may increase the biomagnification potential of an animal beyond diet assimilation and partitioning changes of feces relative to food. One of the simplifying assumptions applied in the original GI model solution was that the mass transport parameter describing chemical flux from gut contents to animal is equal to the mass transport parameter describing flux from animal to its gut contents. This asserts that uptake and elimination flux is diffusion-controlled and coupled throughout the length of the GI tract. However, evidence on hexachlorobenzene bioaccumulation in rats suggested that uptake occurs primarily in the upper GI tract whereas fecal elimination occurs predominately in the colon. Experimental studies on ring doves showed that PCB dietary assimilation efficiencies in ring doves during the uptake phase were higher than feces/animal exchange efficiency measured during the depuration phase. Similar observations were documented in humans.
The fat-flush model and micelle-mediated diffusion model have been suggested as potential submodels for use to augment the GI magnification model. Both the above models are used to explain the phenomena of decoupling of the site and timing of uptake and elimination processes in the GI tract. According to the fat-flush model, fatty acids assimilated by enterocytes of the intestinal mucosa of the small intestine become resynthesized into triglycerides and incorporated into growing chylomicron vesicles. This growth in lipid content of enterocytes increases the partitioning capacity of these cells and temporarily dilutes their chemical potential relative to blood and other body compartments. The lower chemical potential of enterocytes then favors chemical assimilation by diffusion. This process maximizes chemical absorption and minimizes losses of chemical from small intestine cells back to the lumen of the GI tract. When chylomicrons reach a critical size, they are released by active transport from the enterocyte into the circulatory system which again causes a temporary dilution of the blood compartment relative to other body tissues. Following the absorption of dietary lipids
(and assimilated contaminant) from blood by other tissues, the chemical potential of blood once again reequilibrates with other body compartments and becomes maximized. During the fasting state, when chemical potential in blood is highest, fecal elimination becomes more pronounced. At this time, the gut contents are found primarily in the large intestine where fecal elimination has been shown to take place. The fat-flush model therefore describes decoupling in both the site and timing of contaminant assimilation compared to fecal elimination.
The micelle-mediated diffusion model focuses on the physiological role of mixed micelles as vectors for lipid, hydrophobic vitamin and contaminant uptake in the GI tract. Mixed micelles are produced in the intestine as a result of the interaction of bile salts and fatty acids. These amphiphilic vesicles diffuse through the unstirred water layer (UWL) between the gut lumen and intestinal mucosa. Mixed micelles are capable of dissolving long-chain fatty acids, fat-soluble vitamins, as well as other hydrophobic compounds including contaminants in their interiors and transporting these compounds across the UWL. Recent physiological evidence indicates that mixed micelles are unidirectional in their movements between the lumen to enterocyte. A pH microgradient stimulates the breakup of mixed micelles at the interface of the intestinal mucosa of the small intestine. Thus, mixed micelles appear to be involved in the efficient assimilation of hydrophobic contaminants in the upper part of the digestive tract but do not facilitate elimination of chemical from enterocytes back to the lumen of the gut compartment.
Both the mixed-micelle and fat-flush models reflect extensions of the GI magnification model that bring about physiological realism to the digestive process. Current calibration of these models in birds and humans suggests that maximum biomagnification factors may be higher by a factor of 2-4 (i.e., total biomagnification factors ranging from 15 to 20 or higher) than predicted by the original GI magnification model. Calibration of the fat-flush model or mixed-micelle models in fish is yet to be completed. Further research to calibrate maximum bioaccumulation potentials in a wider variety of animal species as well as calibrated animal to gut and gut to animal transfer efficiency terms are required to substantiate these new model predictions and adopt them into food web bioaccumulation models as has been performed with the GI-magnification model.
The earliest critics of biomagnification identified equilibrium partitioning as the main mechanism of bioaccumulation and suggested that the phenomena of food web biomagnification could be explained primarily by differences in whole-body lipid content, and hence chemical partition capacities, of upper-trophic-level animals relative to lower-trophic-level organisms. As described above, food web bioaccumulation data sets generated in the late 1980s and 1990s provided lipid-normalized chemical concentration data and these studies were consistent with the thermodynamic definition of biomag-nification. However, other alternative mechanisms of biomagnification, which do not involve special properties associated with dietary exposures, have been proposed.
Differences in spatially integrated exposures of sampled animals arising due to habitat size and/or differences in migration movements of organisms could potentially result in similar observations as biomagnifica-tion particularly in environments where the contaminant distribution in sediments and water is heterogeneous or subject to point sources. Smaller animals are likely to exhibit small spatial movements and be more reflective of contamination conditions at the local site of capture. Larger animals such as piscivorous fish may exhibit larger spatial movements and consequently integrate chemical exposures over broader spatial scales. Birds may carry residues over very long distances across their migration routes. Indeed the phenomena of biological vectors of pollution related to major spawning migrations of fish and seabirds flying to breeding sites have been recently described. Food web sampling programs for contaminants rarely consider the spatial scale of sample collections as it relates to the potential movements of organisms included within their collections. Spatial movements can confound interpretation of biomagnification factors when all animals are collected from the same location. If animals are collected at a highly contaminated site, food web biomag-nification may appear attenuated as a result of high locally accumulated residues in benthic invertebrates and Zooplanktons. Similarly, biomagnification trends may appear exaggerated when animals are sampled at relatively clean locations but are situated near enough hot spots that some of the larger animals are affected by the more distant contaminated areas.
Similar to the spatial scale described above, temporally explicit exposures may also confound biomagnification observations. Chemical elimination rate coefficients for negligibly biotransformed contaminants are inversely related to body size. Under conditions of pulses in environmental loadings, smaller, lower-trophic-level organisms are more likely to reflect equilibrium with water whereas larger organisms may exhibit lags in their ability to equilibrate with water during or after a pulse. For example, following reductions in water contamination after a seasonal pulse in inputs, as may be experienced during spring melt, phytoplankton and zooplankton may be capable of depurating their residues at a sufficient rate to maintain equilibration with the drop in water concentrations. However, larger fish will take longer to depurate their residues to water and will exhibit both higher concentrations and higher chemical potentials than their zooplankton/plankton counterparts. If the frequency of environmental pulse inputs is faster than the steady-state time of larger fish then this disequilibrium condition may be maintained. For some contaminants which do not achieve steady state in organisms, different animal ages also need to be considered when comparing residues among populations or between populations of species having different age structures.
Another confounding factor arises due to rapid changes in animal lipid contents, either through growth or weight loss. When an animal loses weight and lipids at a faster rate than it can lose contaminant, it concentrates its tissue residues and raises its chemical potential above its previous state even though net chemical flux proceeds in the direction of elimination. Rapid lipid depletion, and subsequent tissue concentration of contaminants, is likely to be common in animals that undergo seasonal cycles of weight gain and lipid loss or in animals that exhibit bioenergetic bottlenecks at critical times in their life history. Such observations were reported in depuration experiments involving birds and fish. In the case of birds, contaminant residues were found to become concentrated in blood following weight losses experienced by the animals during spring warming. The opposite was noted for warm-water fish, the yellow perch, where winter weight losses due to prolonged fasting caused an increase in chemical potential in animal tissues despite the fact that the study was measuring chemical elimination. Other examples documenting rapid weight and lipid loss during specific life-history points and subsequent tissue magnification of PCBs include metamorphosis in amphibians and pipping (hatching) of chicks.
The opposite condition of solvent depletion occurs during rapid growth. Extremely rapid turnover times demonstrated by algae during peaks in primary production result in growth rates that are faster than chemical-uptake coefficients. This causes phytoplankton to exhibit chemical potentials that are lower, and less than equilibrium, compared to water. Rapid growth dilution as experienced in juvenile animals will also reduce biomag-nification factors due to high growth-conversion efficiencies experienced during these life stages.
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