Biologically Mediated Transport of Contaminants to ... - ACS Publications

Critical Review

Biologically Mediated Transport of Contaminants to Aquatic Systems J U L E S M . B L A I S , * ,† R O B I E W . M A C D O N A L D , ‡ DONALD MACKAY,§ EVA WEBSTER,§ COLIN HARVEY,§ AND JOHN P. SMOL| Program for Chemical and Environmental Toxicology, Department of Biology, University of Ottawa, Ottawa, Ontario, K1N 6N5, Canada, Department of Fisheries and Oceans, Institute of Ocean Sciences, Sidney, British Columbia, Canada, Canadian Environmental Modelling Centre (CEMC), Trent University, Peterborough, Ontario, Canada, and Paleoecological Environmental Assessment and Research Lab (PEARL), Department of Biology, Queen’s University, Kingston, Ontario, Canada

The prevailing view is that long-range transport of semivolatile contaminants is primarily conducted by the physical system (e.g., winds, currents), and biological transport is typically ignored. Although this view may be correct in terms of bulk budgets and fluxes, it neglects the potential of animals to focus contaminants into foodwebs due to their behaviors and lifecycles. In particular, gregarious animals that biomagnify and bioaccumulate certain contaminants and then migrate and congregate can become the predominant pathway for contaminants in many circumstances. Fish and birds provide prominent examples for such behavior. This review examines the potential for biovector transport to expose populations to contaminants. In addition, we apply a modeling approach to compare the potential of biovector transport to other physical transport pathways for a hypothetical lake receiving large numbers of fish. We conclude that biovector transport should not be neglected when considering environmental risks of biomagnifying contaminants.

Introduction There is considerable interest in understanding the movement of persistent organic pollutants (POPs) around the globe. Following clear evidence that POPs are transported to regions where they were never used or produced (1), demonstration that they pose risks to environment and human health, and especially indigenous peoples (2), the international community has responded by calling for action to assess the risks and reduce emissions. In some cases, reducing risk has not been easy; many of the chemicals continuing to pose the greatest danger have been banned in the developed world for decades, but large inventories contained in soil, vegetation, water, and ice continue to cycle these chemicals. Although some of these chemicals now fall under the umbrella of the Stockholm Convention of 2001, these contaminants still, in some cases, reach concentrations * Corresponding author phone: (613) 562-5800, ext. 6650; fax: (613) 562-5486; e-mail: [email protected]. † University of Ottawa. ‡ Institute of Ocean Sciences. § CEMC, Trent University. | Queen’s University. 10.1021/es061314a CCC: $37.00 Published on Web 01/06/2007

 2007 American Chemical Society

in fish and mammals high enough to induce toxicity and trigger consumption advisories even in places far from where they were used (1). The study of the fate of toxic chemicals once they have been released from source has historically viewed the environment as a set of fixed boxes (various media) and arrows (fluxes between media, (1)). On a global scale, this conceptual model can be viewed as a large chromatographic system with moving phases (air and water currents), stationary phases (soils, vegetation), and sinks (burial, degradation). This chromatography is further complicated by temperature programming (seasons which produce changes in partitioning resulting in “hopping”), transfers facilitated by the hydrological cycle (snow, rain), and thermodynamic changes in some phases (e.g., metabolism of organic carbon and lipids, melting of snow and ice). Although this simple multi-media box-model concept has been exceptionally helpful for understanding the diverse behavior of many persistent compounds at the global scale (e.g., (3-6)) and has been proposed as a way to screen chemicals for their long-range transport potential (7), other studies discussed in this review are revealing that some pathways, notably biological vectors, subvert the box-model scheme, and can potentially produce surprising risks to target receptor sites. In principle, any contaminant carried within a moving organism constitutes biotransport with, for example, zooplankton vertical migrations broadly moving accumulated chemicals within the ocean. Our discussion in this paper is, however, restricted to a special set of circumstances which leads to unidirectional focusing of a contaminant into a particular location. We call this process biovector transport. Once a contaminant has been distributed into the environment, biovector transport then exhibits three crucial stages: (1) collection of the contaminant; (2) transport and focusing of the contaminant; and (3) deposition, release, or transfer of the contaminant at a receptor site (Figure 1). The omission of any one of these stages arrests biovector transport. In what may be the earliest studies documenting the phenomenon of contaminant biovector transport in migratory fish, Merna (8, 9) observed elevated PCBs and DDT in trout (Salmo spp.) and sculpins (Cottus spp.) which were shown to be feeding on eggs in streams where Lake Michigan coho and chinook salmon (Oncorhynchus spp.) were spawning. The implication was that resident trout and sculpins in streams were acquiring PCBs and DDT accumulated originally by salmon in Lake Michigan. Likewise, higher conVOL. 41, NO. 4, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 1. Moving from left to right, contaminants are released from industrial, municipal, and agricultural regions where they begin to cycle globally. Some of these contaminants transport to the ocean by air or water where they become diluted and widely distributed in the upper ocean through exchange, wet and dry deposition, advection, and mixing. Partitioning into the bottom of the food chain followed by biomagnification up the food chain concentrates contaminants (e.g., PCB, DDT, toxaphene, methyl mercury) into animals (e.g., fish, birds) that forage at sea. Migratory animals then transport and focus these contaminants, sometimes over long distances, to locations where they congregate in large numbers (e.g., spawning rivers, hatcheries) where they then offload some or all of their contaminant burden through feces, molting, or mortality. centrations of mirex were found in resident brown trout (Salmo trutta) in tributaries accessible to migrating salmonids (10). Mercury and methylmercury, which, like the POPs, are volatile, persistent, bioaccumulative, and toxic, should also exhibit biovector transport. A striking example of elevated mercury and mercury-induced mutagenicity in Brazilian forests was produced by migrating birds contaminated with mercury; in particular, ibis (Eudocemus ruber) feathers led to toxic accumulation of mercury in soils (11). In the case described by Merna (8, 9), the collection stage involved the transfer of a broadly distributed, but very dilute, organochlorine reservoir contained in the lake waters into salmon, which was mediated by favorable thermodynamic transfer from water to lipid and by biomagnification up the food chain to approximately trophic level 3. The delivery stage involved efficient mass transport of contaminant burdens to particular natal streams where converging fish offloaded contaminants into lipid-rich eggs. The final stage involved the transfer of contaminants into resident fish opportunistically feeding on a reliable seasonal source of foodsplacing them at trophic level 4. The effectiveness of salmonids as a “biovector transporting system” depends on concentrating the contaminant both by favorable thermodynamic transfers (e.g., partitioning of organochlorines from water into lipid) and by non-thermodynamic concentrating processes (e.g., metabolism of lipids through the food chain and during migration), which Macdonald et al. (12) termed solvent switching and solvent reduction, respectively. In general, contaminant biovector transport is likely to be most significant for substances that biomagnify in foodchains and then are funneled into specific receptor sites as a result of an animal’s social behavior. Over large scales the mass of POPs globally transported by migratory species has been found generally to be smaller than abiotic pathways (air and ocean currents), but biological focusing of contaminants on local scales can surpass the abiotic transport especially at receptor sites where migratory species concentrate following a period of wide dispersal (13). Prominent 1076

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examples of biovector transport derive from migratory fish and birds, though other animals have also been shown to concentrate contaminants along their migratory pathways (e.g., bowhead whales; Balaena mysticetus; (14)). Here we will provide selected examples where migratory animals have affected contaminants in receptor locations and develop a simple model to set biovector transport in the context of other contaminant transporting processes. This approach shows that biovector transport occurs over surprisingly large ranges in distance (from meters to thousands of kilometers) and, due to the collection process, especially selects chemicals prone to bioaccumulation. Finally, we identify knowledge gaps and propose future research for this emerging discipline. Fish (Salmonids) Biovector Transport. Several examples of contaminant biovector transport can be found in the Pacific salmon foodweb. Adult sockeye salmon accumulate more than 95% of their biomass in the ocean and return this biomass to freshwaters when they spawn and die (15). Salmon, which are among the top carnivores in oceans, tend to biomagnify contaminants like PCBs (16). An early example of contaminant biovector transport by Pacific sockeye salmon (17) showed that resident fish (grayling) had higher PCB and organochlorine pesticide concentrations in a lake receiving these salmon compared to a lake receiving no salmon. The similar contaminant pattern in grayling and salmon in the salmon nursery lake led the authors to infer that salmon were the source of POPs to the grayling. In a study of eight Alaskan lakes receiving a range in density of returning Pacific salmon, Kru ¨ mmel et al. (18) showed that anadromous Pacific salmon provided a far more important route of entry than atmospheric deposition for PCBs to some of these nursery lakes. Sediment PCB concentrations in lakes receiving salmon did not exhibit declines after the mid 1990s, as seen in other North American lakes (19), suggesting that curtailing of PCB emissions affects the atmospheric pathway more rapidly than the pathway involving the upper Pacific Ocean and marine salmon. Non-persistent chemicals have also been shown

FIGURE 2. Landsat image of “The Minerets” on Baffin Island. The image highlights a breeding area that includes ∼20 000 pairs of northern fulmars plus kittiwakes and other birds. Chlorophyll reflectance, showing as orange in the figure, highlights productivity associated with the bird colonies. recently to undergo biovector transport. Lipids of Arctic grayling (Thymallus arcticus) in a lake receiving anadromous sockeye salmon have higher concentrations of chlorinated fatty acids compared to those of grayling from a lake without anadromous salmon (20). What makes this latter study especially compelling is that chlorinated fatty acids are unlikely to have significant atmospheric transport potential, making sockeye salmon the only feasible source of contamination in this case. Salmon-derived contaminants can reach beyond aquatic foodwebs. For example, some British Columbia grizzly bears (Ursus arctos horribilis) opportunistically switch from terrestrial food sources to feed on anadromous salmon in late summer (21). This dietary switch has a profound impact on contaminant accumulation by the bears. The authors estimated that salmon deliver 70% of organochlorine pesticides, 85% of the lower brominated PBDE congeners, and 90% of the PCBs for bears that opportunistically feed on these fish (21). An important observation of this study was that the biovector transport process strongly selects contaminants with intermediate hydrophobicity (Kow ∼6.5), which optimizes the combined processes of atmospheric transport, deposition to oceans, biomagnification in the marine foodweb, and transfer from salmon to bears. Mercury biovector transport is notable because a majority of mercury found in carnivores such as salmonids is present as methyl mercury, one of its most toxic forms. For example, Zhang et al. (22) estimated that sockeye salmon have transported over 1 kg yr-1 of methyl mercury to Bristol Bay (Alaska) rivers from the ocean over the past 20 years, which constituted a substantial portion of the rivers methyl mercury budget during this period. Freshwater Chinook salmon (Oncorhyncus tsawytscha) have been observed as vectors for mass transport of mercury in tributaries near Lake Ontario (23). Mercury concentrations in water and suspended particles increased following salmon returns and concentrations were correlated with salmon densities. Concentrations in aquatic invertebrates feeding on salmon carcasses were

25 times higher than those not feeding on carcasses (23). By placing 202Hg labeled perch carcasses on shore, Sarica et al. (24) estimated that about 16% of mercury from the labeled perch was transferred to leeches, and a further 3% transferred to biofilm. The remainder was assumed to have been redissolved into water as aqueous MeHg and some was evaporated from the water body either as dimethyl mercury or as Hg(0) following reduction. Arctic char (Salvelinus alpinus) are widely distributed and migratory (25), thus potentially providing an important biovector for contaminants. However, char do not necessarily die following spawning (iteroparous) and thus fail in the third stage of biovector transport. It is possible that some mortality during freshwater migrations leads to contaminant focusing, but this process would be far less efficient than that associated with fish where mortality always follows spawning (semelparous). Arctic Seabird Biovector Transport. Many studies have observed elevated contaminant concentrations in Arctic seabirds as a result of biomagnification through the marine foodweb (e.g., (2, 26)). Tissue concentrations of contaminants in seabirds vary considerably as a result of differences in trophic position, metabolism, age, physiology, and location (2). There is evidence that organic contaminants affect seabird reproduction (27, 28), immune function, and resistance to parasites (29). Arctic seabirds may also transport significant quantities of marine-derived contaminants from the ocean to terrestrial sites via their guano. For example, annual food consumption by the world’s seabirds is estimated to be about 70 million tonnes, comparable to the total human fisheries harvest of 80 million tonnes (30). In the Arctic, most of these seabirds are high-latitude pelagic feeders who concentrate in very large breeding colonies of >20,000 individuals (31). Many Arctic seabird colony sites are so productive from guano fertilization relative to the surrounding environment that they are visible from satellite Landsat imagery (Figure 2). In a recent study on Bear Island in Norway, the presence of VOL. 41, NO. 4, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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seabird colonies on one lake coincided with elevated PCB concentrations (32), as well as higher chlorobornanes, polychlorinated naphthalenes, and brominated flame retardants (33) in resident fish, which implied that seabird populations are providing a contaminant biovector to some lakes. Note that birds differ from fish in that the former accomplish contaminant deposition predominantly through guano whereas the latter accomplish deposition predominantly through mortality. Local enrichment by nutrients from colonial seabirds has been known for some time (34, 35), but the possibility of local contamination in areas near their nesting sites has only recently been documented (32, 33, 36). Blais et al. (36) showed that a large colony of northern fulmars (Fulmarus glacialis) at Cape Vera on Devon Island in Nunavut (Canada) transport significant quantities of contaminants and nutrients via their guano. These contaminants concentrated in coastal ponds under the cliffs where the fulmars nest. The ponds most affected by seabird guano inputs contained 10-60× higher contaminant concentrations than sediments unaffected by seabirds. The study also noted higher DDE/DDT ratios in sediments near seabird colonies, indicating that DDT and its metabolites in the ornithogenic sediments were more “biologically processed”. In this biovector transport scheme, the efficiency of contaminant transport versus lipids can be dramatically altered depending on factors such as quality of feed and distance to foraging (see for example Gaston et al., (37)). Accordingly, climate-related changes in food sources that lead to increased nutritional stress can also lead to increased contaminant stress via solvent depleting processes due to higher energy expended while foraging (38). Antarctic Seabird Biovector Transport. Antarctic seabirds have received considerable attention recently, in part because these sentinel species provide information on climatic and environmental variability. Fluctuations in the physical marine environment affect resource availability, which in turn affects all marine trophic levels, especially top predators (e.g., (39)). Seabird populations such as penguins and petrels have been observed to fluctuate considerably over the past four decades (40), and sea surface temperatures and sea ice extent have been shown to be among the major forces (41, 42). Abandoned penguin colonies are identified by nest stones, ornithogenic soils, food and body remains, and have been useful for corroborating paleoclimatic records (43, 44). Ornithogenic sediments dating back as much as 3000 years have been analyzed extensively to reconstruct the history of penguin populations in Antarctica (e.g., (45-52)) and sedimentary records in paleo-notches appear to extend that record of penguin population histories even further (53). Elements enriched in penguin guano relative to typical Antarctic soils include sulfur, copper, zinc, cadmium, selenium, strontium, barium, phosphorus, fluorine (45), and 87Sr/ 86 Sr ratios (51). These elements fluctuate considerably and are strongly inter-correlated in sediment cores from Ardley Island, suggesting that these sediment cores track fluctuations in penguin populations through time. Elevated DDT and HCH concentrations have been observed in ornithogenic sediments from Ardley Island (52), providing evidence of contaminant biovector transport by penguins to these locations. In addition to the geochemical tracers described above, novel approaches in molecular biology are being developed to further characterize ornithogenic horizons in lake sediment cores, including analysis of chitinase gene copies using quantitative competitive PCR (54). These ornithogenic lake sediments provide an excellent record for further testing the impacts of biovectors on contaminant distributions in polar regions. Whale Biovector Transport. Little information exists for contaminant biovector transport by whales, but this pathway could be significant. The death of a single 10-70 tonne whale 1078

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could potentially have impacts at the local ecosystem level. Many whales perform migrations as part of their lifecycle, but their specific migratory behaviors vary considerably among species. In spring, most mysticete whales, including the blue, fin, humpback, minke, gray, and right whales, generally migrate from tropical waters to capitalize on the more productive temperate and subarctic seas, and will spend the summer acquiring most of their nutritional reserves there (55). These whales will migrate back to tropical waters in autumn, probably signaled by the shorter daylight cycles. Exceptions include the bowhead whales, which remain in polar waters throughout the year. The odontocete whales, including the sperm, bottlenose, and white whales, also migrate large distances, but their migrations do not always follow annual cycles (55). Some whales migrate thousands of kilometers, thereby acting as potential vectors for long-range transport of contaminants. Odontocetes typically accumulate much more POPs than the filter-feeding mysticete whales, probably due to differences in trophic positioning (56). Both whale varieties accumulate PCB and DDT in blubber to concentrations in the µg g-1 range, with individuals reaching values in the hundreds of µg g-1 (56). The carnivorous killer whales (Orca orcinus) on the western coast of British Columbia, Canada, have high dioxin and PCB burdens, with most individuals above immunotoxicity thresholds for marine mammals (16). Although large numbers of whales do not funnel into small areas where they die like salmon do, individual whales can represent an enormous biomass and nutrient source to scavengers upon mortality. For example, one bowhead whale carcass carries the same biomass as a medium-sized sockeye salmon return to a small nursery lake (Table 1), and may potentially represent an important contaminant source to opportunistic feeders. Importance and Significance of Biovectors Compared to Long-Range Transport. As these examples illustrate, biota such as fish and birds can play a significant role in transporting and distributing POPs in local regions resulting in amplification of concentrations and exposures. As the scale of the region increases, it can be asserted that biotransport, i.e., the mass per day transported in biota, will be less significant than the rates of mass transport in (abiotic) air and water currents. This assertion deserves closer scrutiny for three reasons. First, atmospheric transport of POPs in an airshed or aquatic transport in a river, lake, or oceanic system, flows through the system, so that quantities entering and leaving a region may be large, but thus are usually approximately equal in magnitude. The ecosystem in question is thus “bathed” in contaminated air or water, and will likely approach equilibrium or steady-state with these media. Although the gross rates of contaminant transport in and out may be large, the net rate of input may be small. A notable exception is wet and dry deposition from the atmosphere, especially by snow at high latitudes and altitudes resulting in contaminant accumulation in the snowpack. Subsequent melting can cause an input pulse of contaminant to the ecosystem. Biovector transport, on the other hand, is often fundamentally different in that input is uni-directional, as is the case with spawning salmon or birds nesting on land but feeding from a marine ecosystem. The lack of a corresponding loss route results in contaminant amplification as discussed by MacDonald et al. (12). In terms of fugacity and mass transport (D) values, for an input rate to an ecosystem of f1D1 and an output rate of f2D2, at steady-state f1D1 ) f2D2 and therefore if D1 > D2 then the target ecosystem fugacity, f2, must be amplified over that of its surroundings, f1. Flowing air or water currents are likely to have equal or similar values of D1 and D2, thus f2 will approach f1 and equilibrium is approximated.

TABLE 1. Estimated Bulk Movement from Biovector Transport

species anadromous fish (Pacific) thick billed murre (Uria lomvia) black legged kittiwake (Rissa tridactyla) northern fulmar (Fulmarus glacialis) common eider (Somateria mollissima)

estimated no. of individuals

total migratory biomass (in tonnes)

no. of individuals/area (range)

standard range of annual biomass deposited mass (kg)/area (km-2)

800 milliona

2 milliona

1000 to 40 000b spawners km-2

2500 to 110 000 kg carcasses km-2

1064c km

3 milliond

3000d

Seabirds 2800 to 320 000 individualsj per colony 20 to 60 000 individualse,k per colony 300-100 000e individuals per colony 6-10 000o, e individuals per colony

34 000 to 3.8 millionf kg guano per colony 120 to 360 000l kg guano per colony 3600-1.2 millionf kg guano per colony 70-120 000f kg guano per colony

6000g km

300 000d

82.5d

1 milliond

800d

760 000m

1500n

21 000d

630 000h

1 ha-1

25 000 kg per individual

14 000g km

500 000d

13 millioni

1 ha-1


12 000g km

10 00016

700 000q

1 ha-1


3000 km

Whales sperm (Physeter macrocephalus) gray (Eschrichtius robustus) bowhead (Balaena mysticetus)

maximum distance traveled

3000g km 5000g km 2500g km

a Based on the total Pacific salmon harvested biomass (800,000 tonnes, from (76) multiplied by 2.5). b Based on the highest sockeye salmon return density measured in Alaska by Finney et al. (72). c Salmon migration for Bowron Lake, British Columbia (in Groot and Margolis (76)). d Based on estimates in Wania (13). e Based on Mallory and Fontaine (31). f Based on an estimate of 80 g of guano (wet weight) produced daily per bird (77) for a 5 month nesting season. g Mark Mallory (personal communication). h Based on an estimated mean sperm whale mass of 30 tonnes per individual. i On an estimated mean sperm whale mass of 25 tonnes per individual. j Based on Jones et al. (78), and Birkhead and Nettleship (79). k Based on Suryan and Irons (80). l Based on an estimated 40 g of guano per kittiwake during a 5 month nesting period. m Based on Desholm et al. (81). This number is estimated for Europe only. Number does not include North America, Asia. n Based on an estimated biomass of 2 kg per eider. o Based on estimates from Chaulk et al. (82); largest colony in Canadian Arctic is East Bay (up to 4500 pairs). p Estimated in Environment and Natural Resources Canada: http://www.nwtwildlife.rwed.gov.nt.ca/Publications/speciesatriskweb/bowheadwhale.htm. q Based on an average mass of 70 tonnes per Bowhead whale.

Second, the “mode-of-entry” to the ecosystem is important. It is widely appreciated in multimedia compartmental models, such as a Level III model, that the distribution and fate of a contaminant is strongly influenced by whether it is introduced into air, water, or biota (57). Biovector transport can result in the contaminant entering a food web at a relatively high trophic level; for example, bears feeding on spawning salmon, or aquatic, terrestrial, or avian scavengers feeding on salmon carcasses. In essence, by entering the target or receiving food web directly, the contaminant bypasses the delays and resistances inherent in uptake routes associated with processes such as respiration. Third, biovector transport is of particular significance in cold, high-latitude environments such as the Canadian Arctic which are relatively pristine, but subject to seasonal migrations of birds, fish, and mammals. These organisms are often the source of food for local residents. Arctic ecosystems are often simpler and possibly more vulnerable to disruption by contaminants than temperate or tropical ecosystems that have greater diversity and population densities and less extreme climatic variations. Chemicals that are transported by biovectors into cold climates may also escape some loss processes such as photodegradation. The most convincing demonstration that biovector transport is, or is not, significant would be to quantify contaminant fluxes using a plausible mass balance model and demonstrate agreement with monitoring or empirical data. Not only would such a model be valuable for quantifying the magnitude and dynamics of the biovector transport process, but it could explore which contaminants are likely to be susceptible to biovector transport and to suggest monitoring strategies. Development, calibration, and validation of such models are, however, demanding tasks since both abiotic and biotic components are involved. The food web may be difficult to parameterize or even identify. Conditions usually vary seasonally, thus requiring a dynamic model.

The potential applicability and usefulness of modeling is explored through the development, application, and discussion of a simple, dynamic, model as depicted in Figure 3. The model is based largely on reports that describe the impact of anadromous salmon on nursery lake ecosystems including grizzly bears (19, 21, 58). We emphasize that the model (described in detail in Harvey et al., (59)) is hypothetical and an oversimplification of a very complex set of time-dependent processes. The model lacks realistic time-dependent descriptions of abiotic (seasonal adjustments attributable to temperature, snow, and ice) and biotic (hibernation, migration, metabolism) systems. We apply the model here simply to compare relative importance of the biovector transport pathway, and to discuss how such a model might best be constructed.

Model Description The simulated system consists of air, water, terrestrial, and bottom sediment compartments with relatively pristine air and water inflow typical of a northern region. Outflow is by a river that connects the lake to the ocean. Biotic components consist of a combined terrestrial food source of vegetation, insects, and small animals, and a simple food web of benthic and planktonic organisms, small and large fish, and birds and bears that feed on the fish. Salmon migrate up this river during spawning for approximately a 1-month period. Fish, birds, and bears feed on the salmon during spawning. Uptake and loss by respiration is included, but this is insignificant for birds and bears. Figure 3 illustrates the model in “box” form with arrows indicating the transport and transformation processes that are quantified in the model. The contaminant input processes in the ecosystem are inflows in air, water, and spawning salmon. A differential equation is set up for each compartment and the set is solved numerically to determine the contaminant fate and the contribution of biovector transport. VOL. 41, NO. 4, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 3. Schematic diagram of biotic (oval) and abiotic (rectangular) compartments considered in the model. Arrows represent contaminant transport processes. The mass balance model has three essential components: an abiotic environment, a simple food web, and a spawning salmon component. The model includes four abiotic compartments (see Mackay et al. (60)) and is based on Karluk Lake (Alaska), which has an area of 40 km2, riverine inflows and outflow to the ocean, bottom sediment, surrounding soil, and an overlying atmosphere. There are thus four differential equations in chemical fugacity containing transport and transformation processes. The food web consists of benthos (in equilibrium with the sediment), plankton (in equilibrium with the water), small forage fish that consume plankton, larger fish that consume benthos and small fish, terrestrial food items (vegetation and biota at the average of the soil and air fugacities), birds that feed on large and small fish, terrestrial food, and salmon, and finally, bears that feed on large fish, terrestrial food, and salmon. Mass balance differential equations are written for the two fish species, birds, and bears with the usual parameters of respiration and feeding rates, dietary preferences, lipid contents, and losses by metabolism, egestion, and growth dilution using a formulation similar to that of Campfens and Mackay (61). Salmon migrate from the ocean with a specified fugacity and lipid content. Migration is approximated as a bell-shaped pulse starting in mid-June and lasting until late August, i.e., approximately 70 days. The number of migrating salmon is 17 000 fish/km2, i.e., 680 000 fish entering the 40 km2 lake (19). There is thus a total input of 1700 m3 of salmon over the spawning season. The salmon die, and are consumed or decompose into the water and sediment compartments with a typical residence time after arrival in the lake system of 4 days. The rate of salmon consumption by birds, fish, and bears depends on the prevailing quantity of salmon in the lake, i.e., these predators exploit the opportunity of the available salmon biomass to supplement their normal diet to a defined extent. This is done by calculating a dimensionless availability factor which can range from zero when no salmon are available to 1.0 when the salmon population of the lake is at its maximum. A maximum salmon consumption rate is defined for each predator. The dietary consumption 1080

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of salmon is then the product of these two quantities, namely the availability factor and the maximum rate of consumption. It is assumed that the salmon consumption rate by predators is negligible compared to the natural decay rate. Salmon eaten while in transit to the lake are not considered in the predator diets. The salmon are treated simply as contaminant inputs to the abiotic and biotic compartments of the model and no salmon uptake or loss processes are deduced. A persistent, hydrophobic chemical similar to a PCB with a molar mass of 300 g/mol, KAW of 0.01, log KOW of 6, and negligible degradation and metabolism rates is introduced into the system by three routes: as a constant atmospheric inflow concentration of 0.01 ng/m3, a constant water inflow concentration 0.01 ng/L, and in the spawning salmon with a concentration of 0.018 µg/g wet weight. The model output consists of a complete accounting of all inputs, outputs, fluxes, masses, and concentrations in the compartments at specified time intervals over the year.

Model Results Contaminant levels are expressed as fugacities, which are identical units in all media. Concentrations are proportional to these fugacities but with different proportionality constants or Z values for each compartment. Because there is year-to-year persistence of the contaminant, it is necessary to establish the initial (January 1) condition by “spinning up” to fugacities derived from running the model for a number of years without salmon. This process indicates that there is appreciable carry-over of contaminant from one year to the next, as demonstrated by Kru ¨ mmel et al. (19), and that after 5 years, the abiotic fugacities stabilize. The model shows that fugacities remain constant prior to spawning, a result of constant conditions and feeding rates (Figure 4). As the salmon return to the lake, there is a general increase in contamination in the system. The increase in the fugacity in the water (23%) and sediment (32%) is damped by the large volume of water and the large sorptive capacity of the sediment. The fugacities in fish increase by factors of 3.0-3.6 because of scavenging on dead salmon and uptake from water. The increase in bears and birds is about a factor

The key information provided by the model includes various contaminant mass inputs, likely changes in concentrations as a result of biovector transport, year-to-year carry-over of these concentrations, and source assignment of concentrations in key species. The model serves to synthesize all the available empirical information constrained by a mass balance. The model also assists in monitoring by identifying key variables and likely seasonal variations, for example snowmelt and changes in fat content of biota. A mass balance model can assist in developing a fuller understanding of the complex contaminant distribution and amplification processes in abiotic and biotic systems. Furthermore, the model identifies contaminants that are likely to enter biovector transport pathways and assesses the scale of transport relative to other processes. FIGURE 4. Model results for a persistent bioaccumulating chemical entering the lake through salmon, air, and water. Conditions were initiated by running the model without salmon for 100 years, and then entering salmon for 5 years. of 2.0. In the model system, the small fish exhibit the largest seasonal response to contaminants from salmon followed by large fish (Figure 4). Due to the longer residence times of contaminants, bears show less of a seasonal signal, and there is appreciable year-to-year retention. In reality, the loss of lipids during hibernation may mobilize or concentrate the contaminant but this effect is not included. The magnitude of the various concentration increases is sensitive to the assumed concentration in the salmon, the numbers spawning, and the various parameters describing the diets. The bioaccumulation model indicates that, while contaminant intake increases greatly as a result of feeding on salmon, there is also an increase in the egestion rate which counteracts this increase. Indeed, simulations with a lower concentration in salmon cause a reduction in the concentration in birds and bears because of the increased rates of elimination. The mass contributed by each of the three inputs in the model can be calculated and compared. Atmospheric inputs correspond to an air flow of 7.74 × 1010 m3/h, a concentration of 0.01 ng/m3 and thus a contaminant input rate of some 0.774 g/h or 6785 g/year. The water input flow is 4 × 105 m3/h with a concentration of 0.01 ng/L or 10 ng/m3 thus an input of 4 × 10-3 g/h or 35 g/year. The total salmon input is 1700 m3, i.e., 680 000 fish of volume 2.5 L, with a concentration of 0.018 g/m3 (based on Missildine et al. (58)) resulting in an input of approximately 30 g/year. The atmosphere is the primary source of chemical to the region, however, it is also removing chemical. The mass removed by the atmosphere, the water flow, and by sediment burial in the model are, in the absence of salmon inputs, 6800, 10, and 13 g/year, respectively. With salmon included as an input the removal rates by water outflow and sediment burial all increase to maintain a long-term steady-state. Thus, the advective losses in air and water are approximately equal to the inflows. It is expected that substances that are deposited less reversibly and are retained in soils or water may behave differently. Although the mass input of chemical in salmon is relatively small, it is delivered directly to the food web. This modeof-entry is markedly more efficient than air and water in delivering contaminants. During the spawning season, the fractions of the contaminant concentrations attributable to air, water, and salmon inputs differ among the various compartments. For example, virtually all the contaminant in the air is attributable to inputs from air, whereas water and sediment respond significantly to the salmon inputs. A much greater fraction of the contaminant in bears is attributable to the salmon consistent with the observations of Christensen et al. (21).

Humans as Mediators of Biovector Transport Humans can indirectly mediate biovector challenges to the aquatic environment through the delivery process. Cage farming may impact nutrient dynamics in freshwater and marine systems from feed and fecal production in waters (e.g., (62-64)). Contaminants like mercury, dioxins, PCBs, and brominated flame retardants accumulate in farmed fish from dietary sources (e.g., (65-67)), and these chemicals concentrate near fish pens from fecal egestion and release of excess feed (68), thus closing the biovector pathway by contributing to the deposition phase in these cases. Populations of feral rockfish were recently shown to bioaccumulate high mercury concentrations near salmon farms in coastal British Columbia via this biovector pathway, though other processes, such as higher in situ mercury methylation near salmon pens, are likely active as well (67). Feed additives in aquaculture, such as pharmaceuticals, antibiotics, and dyes, as well as industrial products like antifouling agents, are other potential considerations (69). Recently, on the Alaskan north slope, polar bears (Ursus maritimus) have found it difficult to meet their energy needs due to changes in ice climate which has hindered access to landfast ice (70). As a result, some bears feed opportunistically on bowhead whale (Balaena mystgicetus) carcasses in the Kaktovic area. In this case, human hunting provides the biovector deposition stage, with bears then having an altered exposure to contaminants compared with their normal diet. Ancient examples of human-mediated biovector transport were recently suggested by findings on Somerset Island (Nunavut), where radiometrically dated sediment cores revealed evidence of increased biological productivity in coastal ponds where bowhead whales were flensed by Thule whalers between 1200 and 1600 AD (71), possibly increasing Hg delivery to coastal systems (Blais et al., unpublished data).

Ecological Implications of Biovector Transport Biovector transport concentrates POPs to potentially toxic concentrations and circumvents the standard box budget and flux models by having the potential to transport contaminants over long distances and focus them into critical biological habitats, opening the possibility for contaminants without atmospheric transport potential (chlorinated fatty acids (20), pharmaceuticals, personal care products) to concentrate in remote areas far from emission sources. In many cases described in this review, biovector transport provides the most important contaminant source to specific receptor sites, which we propose will be most significant near large seabird colonies and anadromous fish nurseries (Table 1). Recent examples of biovector transport by seabirds show fish contaminated with 10-40 fold higher PCBs than fish from a nearby lake unaffected by seabird colonies (32), and sediments near fulmar colonies were shown to concentrate DDT and other POPs by up to 60 fold (36). In addition VOL. 41, NO. 4, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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to higher PCBs, fish affected by seabird colonies also exhibited toxicological effects from PCBs, including higher incidences of CYP4501A1 induction (Matt Vijayan, personal communication). The foodweb is a key component of biovector transport because biomass may thus be funneled into a sensitive part of a life cycle (e.g., the nursery), sometimes involving the transporting species itself (fish and bird eggs) and sometimes involving their predators (other fish, bears, birds). Salmon stop feeding during long migrations to spawning sites and, as lipids are converted to energy, PCBs, other POPs, and Hg may be released into the bloodstream where they are subsequently transferred to gonads, liver, and eggs prior to spawning (17). Although large animals, such as bowheads or sperm whales, appear to have a lower potential to focus contaminants through species congregation at a single site, they can, through mortality, provide a large winter “oasis” as carrion for birds, bears, foxes, and other scavengers. In this case, the contaminant exposure to a regional population may depend critically on the contaminant burden carried by a single whale. In some instances, areas of high biological productivity attract the biovector transporting agent (birds, whales, fish). In other instances, biological vectors themselves constitute the dominant source of nutrients. Examples include coastal environments where seabird colonies support an entire ecosystem adjacent to nesting sites by fertilization from guano (32, 36), and where anadromous fish carcasses constitute the dominant source of nutrients to nursery lakes, as seen in parts of Alaska (72). The net result is that this process self-organizes contaminant transport specifically into ecologically important areas. Future research should continue to investigate biovector transport, especially as it relates to contamination of top carnivores like polar bears, whose endocrine function (73), immune function (74), and reproduction (75) have been compromised by POPs. Finally, we note that foodweb structure, migratory pathways, and species distributions are all subject to climate change and variability. Altered risks from biotransport, therefore, are likely to be a strong manifestation of global change and will likely operate in tandem with natural stress incumbent on such change.

Acknowledgments We thank the Natural Sciences and Engineering Research Council of Canada for support. We thank Irene GregoryEaves, Eva Kru ¨ mmel, Mark Demers, and Mark Mallory for collaborations.

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Received for review June 1, 2006. Revised manuscript received November 4, 2006. Accepted November 15, 2006. ES061314A

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