Bioaccumulation of Persistent Organic Pollutants in Lichen−Caribou

Environ. Sci. Technol. 2001, 35, 325-334

Bioaccumulation of Persistent Organic Pollutants in Lichen-Caribou-Wolf Food Chains of Canada’s Central and Western Arctic BARRY C. KELLY AND FRANK A. P. C. GOBAS* School of Resource and Environmental Management, Simon Fraser University, Burnaby, British Columbia, Canada V5A 1S6

While biomagnification of persistent organic pollutants (POPs) in aquatic food chains is well documented, there have been few investigations of the trophodynamics of POPs in Arctic terrestrial food chains. This study presents fieldcollected concentration data and corresponding fugacities of various hydrophobic organic chemicals (ranging in octanolwater partition coefficients or KOW from approximately 103.8 to 109) in two lichen species (Cladina rangiferina and Cetraria nivalis), willow leaves (Salix glauca), barrenground caribou (Rangifer tarandus), and wolves (Canis lupus) from Canada’s Central and Western Arctic region. The results show that, in contrast to aquatic food chains, persistent substances including β-hexachlorocyclohexane and 1,2,4,5-tetrachlorobenzene with a KOW 105 as bioaccumulative substances fail to identify substances that have the potential to biomagnify in Arctic terrestrial food chains despite a low KOW because of a high KOA.

Introduction Since the 1950s, large quantities of organic pesticides such as DDT, hexachlorocyclohexanes (HCHs), hexachlorobenzene (HCB), and dieldrin and industrial-based chemicals such as PCBs have been discharged into the environment. By 1970, observed reproductive effects in the peregrine falcon (Falco peregrinus) were attributed to exposure to organochlorine contaminants (1, 2). DDT, dieldrin, and PCBs were detected in ringed seals from the Norwegian and Canadian Arctic (3). This dispelled the notion that pristine environments such as the Arctic were immune to accumulation of anthropogenic pollutants. Studies investigating the distribution of organic contaminants in aquatic food chains have since shown that some chemicals can biomagnify, resulting in chemical * Corresponding author phone: (604)291-5928; fax: (604)291-4968; e-mail: [email protected]. 10.1021/es0011966 CCC: $20.00 Published on Web 12/07/2000

 2001 American Chemical Society

concentrations in higher trophic level organisms that exceed those concentrations in the organism’s prey (4-8). Many of these compounds are also resistant to chemical degradation, giving them long half-lives in the environment. Long-lived organic contaminants that can biomagnify in food chains and may ultimately cause toxic effects have since been classified as persistent organic pollutants (POPs). Regulatory agencies in Canada, the United States, and Europe have attempted to control the use of first-generation POPs (e.g., PCBs, dioxins, DDT) by either banning or reducing their emission into the environment. Canada’s recently promulgated Toxic Substance Management Policy (TSMP) and the United Nations Environmental Program (UNEP) long-range transboundary air pollution protocol (LRTAP) on POPs have adopted a policy that considers virtual elimination of those chemical substances that meet certain criteria for chemical persistence, bioaccumulation, and toxicity. The bioaccumulation criterion identifies chemicals as being “bioaccumulative” if they exhibit bioaccumulation or bioconcentration factors (BAFs or BCFs) greater than 5000 in aquatic organisms. In the absence of BAF or BCF data, which is often the case, bioaccumulative substances are defined as those compounds with octanol-water partition coefficients (KOW) greater than 105. This criterion is based on the notion that chemicals with KOW values fCARIBOU > fLICHEN).

Methods Overview. Concentrations of several hydrophobic organic contaminants in lichens, caribou, and wolves were compiled through field collections and subsequent analysis and from other sources described below. Concentrations were then expressed in terms of fugacities (see Fugacity Analysis) and compared by applying the statistical methods outlined below. Lichen Samples. As part of the present study, two common lichen species (Cl. rangiferina and Ct. nivalis) were collected at several locations in close proximity to Bathurst Inlet (64°15′ N, 113°07′ W) and Cambridge Bay (69°07′ N, 105°03′ W) (Figure 2). During the spring of 1997 (i.e., May-June), Cl. rangiferina and Ct. nivalis samples were collected east and west of Bathurst Inlet along the Huikitak and Hood Rivers, respectively. During the summer of 1998 (i.e., July), additional samples of Cl. rangiferina and Ct. nivalis east and west of Bathurst Inlet were obtained near the communities of Omingmaktok (east) and Brown Sound (west), while at Cambridge Bay only Ct. nivalis samples were collected. Vegetation samples were identified using ref 22. At each sampling location, 3-6 independent samples of lichens and/ or willow leaves were collected for chemical analysis. The air 326

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temperature during the lichen and willow leaf collections ranged between 20 and 25 °C during both the spring and summer collection periods. Samples were stored at -10 °C in 5-mL glass vials. Lichens and willow leaves were washed with distilled water before chemical analysis to remove loosely bound particulate matter. Preparation and cleanup of vegetation samples (this study) were performed at the Great Lakes Institute of Environmental Research (GLIER) according to Lazar et al. (23). Lichen and willow leaf samples (approximately 10 g wet wt/sample) were homogenized with 20 g of Na2SO4 using a glass mortar and pestle. The homogenate powder was transferred to a Na2SO4 column, spiked with Surrogate Spiking Standards (1,3,5-tribromobenzene, tetrachloro-m-xylene, and PCB 209), and then extracted by eluting with 50 mL of hexane. The extract was collected and evaporated to 2 mL. A 2-mL sample of dichloromethane (DCM) was then added to this extract and transferred to a gel permeation column (GPC) filled with 50 g of BioBeads S-X33 (Bio-Rad) in 50% DCM/hexane solution (v/v). The lipid fraction from the GPC was collected and discarded. The remaining 150 mL of eluent from the GPC was collected and transferred to a 1 × 35 cm glass column prepared with 6 g of Florisil (60-100 µm mesh) topped with 2 cm of anhydrous Na2SO4. Three fractions were eluted using hexane (fraction 1), 15% DCM/hexane (fraction 2), and 50% DCM/hexane (fraction 3). Each fraction was evaporated to 2 mL and analyzed using a Hewlett-Packard model 5890 gas chromatograph with electron capture detection (GC-ECD). Chemical identification and quantification were performed by comparing the sample peak against the respective peak areas in calibration standard solutions (obtained from the Canadian Wildlife Service Laboratory, Hull, PQ, Canada) for each of the three fractions. Method blanks, consisting of Na2SO4, were extracted according to the same procedure as environmental samples and analyzed with every batch of 6 samples to check for contamination of the extracts. The method detection limit (MDL) was determined by analyzing 8 solutions of corn oil spiked with the target chemicals at a concentration exceeding the instrument detection limit by at least 10-fold. The MDL was then determined as the mean concentration plus 2.4 times the standard deviation. The extraction recovery efficiencies (based on recovery of spiked surrogate standards) were all greater than 90%. The lipid content was determined on

FIGURE 2. Map of the study area depicting the collection sites of lichens, willow leaves, caribou, and wolves near Bathurst Inlet, Cambridge Bay, and Inuvik. subsamples of the extracts and reported as a percentage of the sample’s wet weight. Moisture content was determined by comparing the sample’s wet and dry weights after ovendrying 1 g of sample at 125 °C for 24 h. Total organic carbon (TOC, % of dry tissue) of the dried lichens and willow leaves were determined by combustion/nondispersive infrared gas analysis using a Shimadzu 5050A TOC analyzer. TOC is calculated as the difference between measured total carbon and total inorganic carbon. From 1992 to 1995, the Government of the Northwest Territories (GNWT) also collected samples of Cl. rangiferina and Ct. nivalis from Bathurst Inlet, Cambridge Bay, and Inuvik (68°18′ N, 133°29′ W) for chemical analysis (see Figure 2). The methods of analysis and observed concentrations of organochlorines in lichens from the GNWT study have been summarized in the 1998 Arctic Monitoring and Assessment Program’s (AMAP) Assessment Report (24). All measured concentrations in those lichen samples were provided by the GNWT. Concentrations in lichen samples from Bathurst Inlet, Cambridge Bay, and Inuvik were compiled from both data sets and separated by species and sampling location. Because lichens from the Bathurst region were collected during spring and summer months, concentrations for those lichens were also separated by season. Concentrations on a dry weight basis (ng/g dry wt) were determined by dividing

the wet weight chemical concentrations by the dry matter content (DM) of each sample. Caribou and Wolf Samples. Between 1992 and 1995, the GNWT collected male and female caribou from the Bathurst, Bluenose, and Victoria Island caribou herds (see Figure 2). Also during their study, the GNWT collected male and female wolves on the range of these caribou herds. Organochlorine concentrations in liver, muscle, and fat tissues obtained from individual caribou and wolves at these locations were analyzed at the GLIER facilities and are summarized in refs 24 and 25). The chemical concentration data (provided by the GNWT) were separated by tissue type, collection site, sampling date, and sex. Because caribou from Bathurst Inlet were collected during summer (July) and fall (September), the chemical concentrations observed in tissues of Bathurst caribou were further separated by season. The sex of wolves sampled at Inuvik was not determined; hence, concentrations for these animals could not be separated by sex. Also, no separation of concentrations by season was possible for wolves at all three locations because sampling of these animals only occurred in the fall (October-November). Wet weight concentrations were lipid normalized (ng/g lipid wt) by dividing by the lipid content of each sample. Fugacity Analysis. Chemical fugacities ( f, in Pa) were calculated from observed concentrations (C, in mol/m3) and VOL. 35, NO. 2, 2001 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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corresponding fugacity capacities (Z, in mol m-3 Pa-1) of a given medium, as f equals C/Z. Fugacities in caribou and wolf tissues were calculated as the lipid-normalized concentration in a given tissue (in mol/m3 lipid) divided by the fugacity capacity of lipid (ZL). The fugacity capacity of lipid is assumed to be equal to the fugacity capacity of octanol (ZO) and is calculated as ZL ) KOWZW. KOW is the octanolwater partition coefficient, and ZW is the fugacity capacity of water, which is the reciprocal of the chemical’s Henry’s law constant (HLC, in Pa m3 mol-1). Fugacity capacities in caribou and wolves were calculated at 20 °C, hence ignoring the difference in temperature between the animal’s tissues and the temperature at which KOW and HLC were determined. Fugacities in lichens and willow leaves were calculated at the field sampling temperature (20-25 °C) as the chemical concentration measured in those samples (mol/m3 dry tissue) divided by the respective fugacity capacities of lichens (ZLICHEN) and willow leaves (ZLEAF). The fugacity capacities of the lichens and willow leaves were approximated as φOCdL × 0.35KOW/HLC and φOCdW × 0.35KOW/HLC, respectively, where dL and dW are the densities of the lichens (i.e., 0.64 kg/L) and willow leaves (i.e., 0.89 kg/L) and φOC is the organic carbon content of the lichens or willow leaves. This method of calculation assumes that the organic carbon fraction of the lichens and willow leaves is the predominant phase in which hydrophobic organic chemicals partition and that the organic carbon matter in lichens and leaves can be represented as 35% of octanol following Seth et al. (26). This method was selected over a “lipid partitioning model” because lichens and willow leaves contain very low lipid contents (approximately 0.5% and 1%, respectively) and extremely high organic carbon contents (approximately 20% and 40%, respectively), indicating that the organic carbon fraction of these organisms provides the majority of the sorptive capacity of these vegetative materials. An organic carbon partitioning based model has also been suggested for aquatic algae (27, 28). Lichens are a symbiosis involving an alga and a fungus. The Z values calculated by this method are consistent with those in azalea leaves reported by Paterson et al. (29), who suggested that Z values for plant leaves can be approximated by a model that views the partitioning properties of vegetative materials as 5% of KOW. It should be stressed that observations in vascular plants (30, 31) indicate that plant materials can vary significantly in their partitioning properties and that reliable models for the estimation of plant-air partition coefficients and corresponding Z values for plants have not been developed to date. Hence, the fugacity capacities for lichens and willow leaves may be subject to error and should be treated with caution. KOW values and HLCs of individual compounds used for calculating Z values were compiled from refs 32-34. All fugacity values are reported as nPa, i.e., 10-9 Pa. Statistical Analysis. Fugacities exhibited log-normal distributions and were hence transformed logarithmically to determine the geometric means (GM) and the standard deviation of the geometric mean (SDG). In Tables 1 and 2 (see Supporting Information), the SDG is presented as 10SDG. One-way analyses of variance (ANOVA) tests were performed on calculated log-transformed fugacities to determine statistically significant differences between the geometric means of fugacities in lichens, caribou, and wolves.

Results and Discussion Bioaccumulation in Lichens. Chemical concentrations and corresponding fugacities in lichens and willow leaves from sampling locations in Canada’s Central and Western Arctic are listed in Tables 1a and 1b, respectively (see Supporting Information). Lipid contents, moisture contents, HLC, KOW, KOA, ZLICHEN, and ZLEAF values are also presented in Table 1. The mean lipid content of lichens and willow leaves on a dry 328

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weight basis was 0.45% and 1.05%, respectively. The measured organic carbon content of dried samples of Cl. rangiferina, Ct. nivalis, and S. glauca were 42.9%, 35.4%, and 20.8%, respectively. The density of lichen and willow leaves was 0.64 and 0.89 kg/L, respectively. The principal contaminants detected in vegetation samples (Cl. rangiferina, Ct. nivalis, and S. glauca) were R-HCH, γ-HCH, HCB, p,p′-DDT, and PCB congeners 153, 138, 110, 101, 118, 170/190, and 66/95. Figure 3 shows that fugacities of organochlorines such as R-HCH, γ-HCH, and HCB were greater than fugacities of PCBs (illustrated with congener 153) in vegetation samples at all sampling locations. At some locations, samples of Ct. nivalis, Cl. rangiferina, and S. glauca exhibited statistically different fugacities of R-HCH, γ-HCH, HCB, and PCBs (e.g., Inuvik, Brown Sound, and Cambridge Bay). There were no statistically significant differences in fugacities of R-HCH, γ-HCH, HCB, and PCBs in lichens and willow leaves collected during the summer (i.e., between summer sampling locations). This indicates that the spatial distribution of these contaminants is fairly homogeneous, possibly reflecting atmospheric concentrations. The available data indicate that differences in chemical concentrations among the various food items in the caribou diet are small during summer months. Figure 3 illustrates that the fugacities of PCB 153 in Cl. rangiferina samples collected near the Hood River during May were significantly (i.e., 75-250 times) greater than fugacities of PCB 153 in the same lichen species collected in July at the other summer sampling locations while the temperature during the lichen collection in May and July was approximately the same (i.e., between 20 and 25 °C). Similarly, the fugacity of PCB 153 in Cl. rangiferina and Ct. nivalis samples collected near the Huikitak River during the spring were 23-178 times greater than fugacities of PCB 153 observed in those lichen species collected during July at nearby locations. Various other PCB congeners demonstrated comparable fugacity increases in spring-collected lichens relative to lichens collected during summer (see Table 1b in Supporting Information). Statistically significant differences between fugacities in lichens collected in May and July were also observed for R-HCH, γ-HCH, and HCB, but differences were smaller than those for PCBs. The apparently larger fugacities of these organochlorine contaminants in lichens during the spring as compared to the summer may be due to accumulation of these substances in spring meltwater and subsequent uptake in lichens. Collection of lichen samples in the spring of 1997 (i.e., Hood and Huikitak River samples) occurred during the spring snowmelt period. Snowpacks contain contaminants scavenged during the previous winter’s snowfall events (35-37). Snow sublimation tends to “concentrate” these contaminants in the snowpack, especially for low volatile PCBs that evaporate very slowly from the snowpack. The more volatile HCHs and HCB evaporate more rapidly, reducing their degree of snowpack accumulation. During snowmelt events, when snow turns into meltwater, a significant drop in the fugacity capacity may further elevate the fugacity in meltwater over that in the snowpack. The meltwater is in direct contact with lichens during this period. Exchange of contaminants between lichens and meltwater may therefore explain greater lichen fugacities in the spring as compared to those in the summer when lichen-air exchange processes control lichen fugacities. Data from ref 24 show that ∑PCB concentration (based on 90 congeners) in Arctic air over a 2-yr period ranged from 7.6 to 18.9 pg/m3 or 0.05-0.3 nPa, while the fugacity of ∑PCBs (based on 43 congeners) in spring-collected lichens ranged between 0.6 and 1 nPa. This indicates that the elevated fugacities in lichens during the spring cannot be explained solely by seasonal fluctuations in temperature and/or contaminant air concentrations and points toward the role of snowpack ac-

FIGURE 3. Fugacities (nPa) of r-HCH, γ-HCH, HCB, and PCB153 in two common lichen species (Cl. rangiferina and Ct. nivalis) and tundra willows (S. glauca) from various sampling locations in Canada’s Central and Western Arctic. Data are presented on log scales and are reported as geometric means. Error bars represent the standard deviation. ND indicates nondetectable concentrations during chemical analysis. An asterisk (*) indicates statistical significance (p < 0.05) between mean chemical fugacities in lichens collected in spring (Huikitak and Hood River samples) as compared to lichens collected nearby in summer (Omingmaktok, Brown Sound, and mid-Bathurst samples). Two asterisks (**) indicate a statistically significant difference (p < 0.05) between vegetation species at a given sampling location. cumulation of contaminants. Concentrations of ∑PCBs (based on 116 congeners) in snowpacks from the Central Arctic (24) were approximately 4.1 ng/L snow and equivalent to 4.6 ng/L water, corresponding to a substantial ∑PCB fugacity of 190 nPa in meltwater. These data suggest that organic chemicals can attain relatively high fugacities in melting snowpacks, causing equilibrium partitioning with spring meltwater to be an important mechanism for contaminant uptake in lichens. Bioaccumulation in Barren-Ground Caribou. Tables 2a and 2b in the Supporting Information illustrate that the predominant compounds detected in caribou tissue samples were R-HCH, β-HCH, 1,2,4,5-TCB, HCB, oxychlordane, p,p′DDE, and PCB congeners 118, 138, 153, and 180. The fugacities of chlorobenzenes (1,2,4,5-TCB and HCB) and HCHs (R and β isomers) were greater than those of PCB congeners and organochlorine pesticides. While wet weight concentrations varied by orders of magnitude, fugacities in liver, muscle, and fat tissues of caribou were comparable and not statistically different. For example, HCB in liver, muscle, and fat tissues of Bathurst male caribou in September exhibited fugacities of 14.5, 14.9, and 19.1 nPa, respectively, while HCB concentrations in those tissues were 0.52, 0.15, and 8.12 ng/g wet wt, respectively. The similarity of fugacities in liver, muscle, and fat tissue indicates that tissue concentrations in caribou are close to an internal chemical equi-

librium. Because the higher chemical concentrations in fat tissue samples contain smaller analytical error than the lower concentrations in liver and muscle tissue samples, fat concentration data were used to determine the fugacities in caribou for the biomagnification analysis. The fugacities of HCHs, DDTs, chlordanes, chlorobenzenes, and PCBs in the tissues of male caribou from Bathurst Inlet were significantly (p < 0.05) greater in the summer than in the fall, e.g., 135 nPa for HCB in July and 19 nPa in September. The observed drop in chemical fugacities (by approximately a factor of 7) between the summer and the fall can be explained by increased lipid production and growth. In the Arctic, caribou gain substantial deposits of fat and protein over the short summer period to utilize energy during the winter, resulting in greater body weights in the fall as compared to early summer (38, 39). A study involving a 12-week feeding experiment of captive caribou showed that caribou gain between 30 and 40 kg of ingesta-free body weight between May and August (40). Over the same period, the content of fat tissue as a percentage of body weight increased from 5 to 18%. This corresponds to a 4-5-fold increase in the amount of body fat, which tends to “dilute” the chemical concentration in the fat. However, this degree of dilution can only be accomplished if no net uptake of chemical occurs. The fact that a 7-fold drop in the HCB fugacity in the male caribou occurred given an approximately VOL. 35, NO. 2, 2001 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 4. Fugacities (nPa) of individual compounds from various classes of POPs in lichen-caribou-wolf food chains at Bathurst Inlet, Cambridge Bay, and Inuvik. Data are presented on log scales, where bars represent the GM of chemical fugacities in lichens Cl. rangiferina and Ct. nivalis in summer, caribou during fall (males and females), and wolves during fall (males and females). The left-hand scale is for HCHs and chlorobenzenes (CBz). The right-hand scale is for DDTs, PCBs, and chlordanes. Error bars represent the standard deviation. ND indicates nondetectable concentrations during chemical analysis. An asterisk (*) refers to statistically significant biomagnification for the lichen-caribou trophic transfer (i.e., fCARIBOU > fLICHEN), while two asterisks (**) represent statistically significant biomagnification for the caribou-wolf transfer (i.e., fWOLF > fCARIBOU). 4-5-fold increase in fat content suggests that there is no net uptake and perhaps even some depuration of HCB between the summer and the fall. This agrees with the observation that lichen concentrations and fugacities during the summer are 100-fold less than in spring after snowmelt. Male caribou may obtain the majority of their POP body burden during the spring, when lichen concentrations are high, and throughout the period between the spring and the fall slowly eliminate a significant fraction of their body burden. Fugacities of POPs in female caribou from the Bathurst herd during the summer were significantly lower (p < 0.05) than those in males (e.g., 21 nPa for HCB in females and 135 nPa for males). This may be due to chemical elimination through lactation throughout the nursing period. On the Bathurst range, calving occurs in early June, and nursing continues until the calves are weaned in August or September. Lactation has been proposed as an explanation of the lower levels of hydrophobic contaminants in female mammals in other species (5, 8, 41). The fugacities of POPs in female caribou did not significantly drop between summer and fall despite an observed 3-fold increase in lipid content of fat tissue in these animals over this period (Table 2b in Supporting Information), e.g., 21 nPa for HCB in July and 19 nPa in September. The results indicate that because fugacities in female caribou are much lower than in males (due to lactation), POP-contaminated lichen consumption by female 330

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caribou resulted in net chemical uptake while the males (with higher tissue fugacities) eliminated POPs through fecal egestion. The net uptake in the females is compensated by lipid growth dilution of equivalent magnitude, resulting in no change in fugacity over time. Bioaccumulation in Wolves. R-HCH, β-HCH, 1,2,4,5-TCB, HCB, oxychlordane, and PCB congeners 153, 138, and 180 were the predominant compounds observed in wolf tissues. Similar to caribou, fugacities of most compounds in liver, muscle, and fat tissues of wolves were not statistically different, indicating an internal chemical equilibrium among the internal tissues of wolves. For example, the fugacity of PCB 180 in liver, muscle, and fat tissues of male wolves from Bathurst Inlet were 0.013, 0.017, and 0.020 nPa, respectively. No statistical differences in chemical fugacities were detected between male and female wolves. However, chemical fugacities in Bathurst adult wolves (>2 yr) were significantly greater (p < 0.05) than those fugacities in young wolves (2 yr (the dark filled circles) were separated from the pooled population of male and female wolves (white circles) because they were statistically different (p < 0.05). Similarly, BMFs for Cambridge Bay males (gray circles) were separated for the same reason. of wolves are primarily related to prey availability and prey abundance (42-44). When wolves inhabit the range of barren-ground caribou herds, they have been observed to primarily prey on readily available caribou (20, 21). The Bathurst and Bluenose ranges contain abundant caribou populations. However, Victoria Island sustains a sparsely populated caribou herd. Wolves on Victoria Island likely feed predominantly on more available prey species such as ptarmigan (Lagopus mutus), Arctic hare (Lepus arcticus), and or muskoxen (Ovibos moschatus). A recent summary of terrestrial ecosystem contamination in the Arctic (9) indicates that these species exhibit lower concentrations of POPs than caribou from the same region. For example, fat tissue concentrations of HCB in ptarmigan, Arctic hare, and caribou sampled near Arctic Bay (Baffin Island) were 0.3, 11, and 57 ng/g (wet wt), respectively. Also, HCB concentrations in fat tissue of the relatively abundant muskoxen inhabiting Victoria Island (14.3 ng/g wet wt) reported in ref 11 were lower than HCB concentrations in caribou (32.8 ng/g wet wt) sampled on Victoria Island in the same season. Substitution by Victoria Island wolves of the more contaminated caribou for less contaminated prey species may be the reason for the apparently lower BMFs observed in wolves from Cambridge Bay. 332

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BMF Relationships with KOW and KOA. Figure 5 shows BMFs in male and female caribou and wolves from various locations relative to log KOW and log KOA. KOW is of fundamental significance in the bioaccumulation of hydrophobic organic substances in aquatic organisms because the BMF of nonmetabolizable substances is the result of competing rates of chemical uptake from the gastrointestinal tract (GIT) and elimination to the water, which correlates with KOW (45, 46). However, in terrestrial mammals, the octanol-air partition coefficient (KOA) is of greater importance than KOW since the BMF for nonmetabolizable hydrophobic substances is mainly the result of competing rates of chemical uptake from the GIT and elimination to the air. Figure 5a, showing all observations, illustrates that there is a large variability in observed BMFs of the various substances. Relationships between BMF and KOW and KOA are difficult to discern from these figures. Assuming that the capability of caribou and wolves to metabolize some substances but not others is a key factor causing the variability in BMF seen in Figure 5a, we removed those substances that are believed to be metabolized in Figure 5b,c. Metabolizable substances were considered to be those substances for which fB/fD was less than 1.0. They included PCB congeners 52, 101, 105, 118, etc. that have vicinal hydrogen atoms in ortho-meta or meta-

para positions and have previously been associated with metabolic transformation in mammals (47). Figure 5b shows that in caribou the BMF does not vary in a statistically significant fashion with KOW over a log KOW range between approximately 3.5 and 8. A similar trend is observed when the BMFs are plotted versus KOA (Figure 5c); however, a small (3-4-fold) statistically significant decline of the BMF with increasing KOA (104-fold) becomes apparent. This relationship may reflect the role of the intricate ruminant system of caribou to absorb nutrients (and also contaminants) from a substrate that is difficult to digest. This ruminant system optimizes the exchange of contaminants between the caribou’s tissues and the GIT causing exhalation to be an insignificant route of elimination (compared to fecal egestion). For this reason, the BMF in caribou is rather independent of KOA. The small drop in BMFs in caribou with increasing KOW (Figure 5b) and KOA (Figure 5c) is likely due to the reduction in GIT uptake rate and hence absorption efficiency (EA) for more lipophilic substances (log KOW > 6.0), which has been observed in fish (48, 49), rats (50), humans (51, 52) and cows (53). For caribou, it appears that the drop in EA for high KOW chemicals is very large as compared to the expected drop in the lipid-to-air elimination rate (via exhalation) with increasing KOA, thereby causing lower BMFs for higher KOA compounds. This is in agreement with McLachlan (53), who observed a substantial 5-fold drop in EA of POPs in ruminant dairy cows (i.e., EA decreased from 80% to 15% over a log KOW range of 5.0-8.0). Figure 5b,c shows statistically significant increases in the BMF in wolves with increasing KOW and KOA. Wolves exhibit a 10-20-fold increase in BMFs over a 104-fold increase in KOA. Correlations between wolf BMFs and KOA are considerably better than those with KOW (Figure 5b), as illustrated by the higher correlation coefficients. The data suggest that wolves have an efficient digestive system in which digestion of an easily digestible lipid-rich diet generates a high degree of GIT magnification in the GIT (resulting in a large fugacity gradient between the GIT and the organism) and consequently a high GIT uptake rate. This high uptake rate is counter-balanced by elimination to the air (via exhalation). Thus, high KOA substances being eliminated more slowly than those with a lower KOA exhibit higher BMFs. The less than proportional increase of the BMF with KOA likely reflects that the gastrointestinal to organism rate constant and hence EA drops with increasing KOW (which correlates with KOA). Bioaccumulation studies in rats (50) and humans (51, 52) have shown that EA of high KOW substances in those organisms decreases from 98% to 70% over a log KOW range of 5.0-8.5. EA in wolves can be expected to follow a similar behavior. The high GIT uptake rate in wolves is therefore expected to drop slightly with increasing KOA but at a slower rate than the elimination rate to air falls with increasing KOA, resulting in a less than proportional relationship between the BMF and KOA. While bioaccumulation studies of aquatic organisms and food chains (54-56) have consistently shown that organic substances with log KOW values less than 5 do not biomagnify in the food chain, this study illustrates that in the lichencaribou-wolf food chain a substantial degree of biomagnification occurs for chemicals with a log KOW as low as 3.8. In relation to other organic contaminants, β-HCH and 1,2,4,5TCB that have low KOW values (i.e., log KOW of 3.8 and 4.7, respectively) also have low Henry law constants, thereby exhibiting relatively high KOA values. Chemicals with high KOAvalues (due to relatively high KOW and low HLCs) tend to show considerable biomagnification in food chains that include mammals. Other studies confirm this notion. For example, BMFs equal to 7.6 and 2.0 were reported for ∑HCH (log KOW ) 3.81) in ringed seals (Arctic cod/blubber) (24) and beluga whales (Arctic cod/blubber) (57). Also, R-endosulfan

(log KOW ) 3.83) has been observed to biomagnify in beluga whales and in ringed seals (57). HCHs and R-endosulfan both exhibit relatively low HLCs and therefore a relatively high KOA. The significance of a high KOA for terrestrial biomagnification is that lipid-to-air elimination (through exhalation) is low, causing, in absence of metabolic transformation, a very low depuration rate to counteract uptake from the GIT, hence resulting in high tissue concentrations (and fugacities) in mammals. Implications for Developing POPs Bioaccumulation Criteria. The current international protocol on POPs and management policies for POPs in Canada only consider chemicals with a log KOW > 5 as being bioaccumulative. A chemical is considered to be bioaccumulative if it biomagnifies in the food chain. This study shows that these policy instruments do not contain adequate criteria to identify substances that biomagnify in Arctic terrestrial food chains. The latter is somewhat ironic, as the policies and protocols on POPs have primarily been developed with the goal to protect remote northern ecosystems and communities. To prevent the presence of bioaccumulative substances in Arctic terrestrial food chains, it is imperative that bioaccumulation criteria are developed with the goal to identify chemical substances that are bioaccumulative in both aquatic and terrestrial food chains. Our analyses of BMFs in caribou and wolves indicate that gastrointestinal absorption efficiencies and lipid-to-air elimination rates, which are strongly dependent on the chemical’s KOW and KOA, respectively, are two important parameters affecting POPs biomagnification in these animals. It is important to note that different animal classes (e.g., herbivores and carnivores) are expected to exhibit differences in these two parameters due to their distinct taxonomic and physiological characteristics. Our findings also demonstrate that BMFs for individual animals can differ substantially with differences in gender, age, season, and dietary preferences. Consequently, the extent of bioaccumulation of organic chemicals in terrestrial food chains is not only controlled by physical-chemical properties such as KOW and KOA but also strongly depends on aspects of physiology, time, food web characteristics, and predatorprey interactions at each trophic transfer. There is currently insufficient information regarding bioaccumulation processes in terrestrial mammals to select a predetermined KOA threshold criterion for assessing terrestrial food chain bioaccumulation potential. Therefore, we propose an approach involving the development and application of mechanistic bioaccumulation models for mammalian species and food chains to aid in selecting bioaccumulation criteria that is specific to mammals, and that aims to protect all organisms at all life stages. This approach may also be useful for quantifying contaminant levels in animals of “high risk” categories (e.g., newborns, top-predators), which would aid in assessing the toxicological hazard of existing chemicals. Also, further investigation into routes of exposure and elimination of “low” KOW but “high” KOA substances in mammals (e.g., respiratory elimination, GIT to organism partitioning) may elicit new insights into understanding the mechanisms of biomagnification of POPs in terrestrial food chains.

Acknowledgments We thank Drs. Rodica Lazar and Douglas G. Haffner of the Great Lakes Institute of Environmental Research (GLIER) for assistance in the chemical analysis of vegetation samples. We also thank Drs. Brett Elkin and Colin Macdonald for providing access to organochlorine concentrations in lichens, caribou, and wolves. We acknowledge the financial support of the Natural Sciences and Engineering Research Council of Canada, the Association of Canadian Universities for Northern Studies, and Simon Fraser University’s Northern Science Training Program. VOL. 35, NO. 2, 2001 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Supporting Information Available Two tables showing the GM of concentrations and corresponding fugacities of various organic chemicals observed in lichen and leaves of the willow and observed in liver, muscle, and fat tissue of caribou and wolves (40 pages). This material is available free of charge via the Internet at http:// pubs.acs.org.

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Received for review April 19, 2000. Revised manuscript received October 12, 2000. Accepted October 13, 2000. ES0011966