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Assessing Trace-Metal Exposure to American Dippers in Mountain Streams of Southwestern British Columbia, Canada

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Assessing Trace-Metal Exposure to American Dippers in Mountain Streams of Southwestern British Columbia, Canada Environmental Toxicology and Chemistry, Vol. 24, No. 4, pp. 836±845, 2005 q 2005 SETAC Printed in the USA 0730-7268/05 $12.00 1 .00 ASSESSING TRACE-METAL EXPOSURE TO AMERICAN DIPPERS IN MOUNTAIN STREAMS OF SOUTHWESTERN BRITISH COLUMBIA, CANADA CHRISTY A. MORRISSEY,² LEAH I. BENDELL-YOUNG,² and JOHN E. ELLIOTT*³ ²Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A 1S6, Canada ³Canadian Wildlife Service, Environment Canada, 5421 Robertson Road, Delta, British Columbia V4K 3N2 (Received 1 March 2004; Accepted 8 September 2004) AbstractÐTo develop a suitable biomonitor of metal pollution in watersheds, we examined trends in exposure to nine trace elements in the diet (benthic invertebrates and ®sh), feathers (n 5 104), and feces (n 5 14) of an aquatic passerine, the American dipper (Cinclus mexicanus), from the Chilliwack watershed in British Columbia, Canada. We hypothesized that key differences may exist in exposure to metals for resident dippers that occupy the main river year-round and altitudinal migrants that breed on higher elevation tributaries because of differences in prey metal levels between locations or possible differences in diet composition. Metals most commonly detected in dipper feather samples in decreasing order were Zn . Cu . Hg . Se . Pb . Mn . Cd . Al . As. Resident dipper feathers contained signi®cantly higher mean concentrations of mercury (0.64 mg/g dry wt), cadmium (0.19 mg/g dry wt), and copper (10.8 mg/g dry wt) relative to migrants. Mass balance models used to predict daily metal exposure for dippers with different diets and breeding locations within a watershed showed that variation in metal levels primarily was attributed to differences in the proportion of ®sh and invertebrates in the diet of residents and migrants. In comparing predicted metal exposure values to tolerable daily intakes (TDI), we found that most metals were below or within the range of TDI, except selenium, aluminum, and zinc. Other metals, such as cadmium, copper, and arsenic, were only of concern for dippers mainly feeding on insects; mercury was only of concern for dippers consuming high ®sh diets. The models were useful tools to demonstrate how shifts in diet and breeding location within a single watershed can result in changes in exposure that may be of toxicological signi®cance. KeywordsÐMetals Feathers Feces American dipper Ecological risk assessment INTRODUCTION model for monitoring metal pollution in mountain streams be- Trace metals are present in aquatic systems worldwide, cause they integrate contaminant sources from their aquatic largely from underlying substrates, natural erosion, volcanism, diet over time and space. and hydrological cycles. However, mining processes [1], urban Previous studies in the Chilliwack watershed of British Co- and agricultural runoff [2], industrial emissions [3], and de- lumbia revealed that American dippers have distinct altitudinal forestation [4] also can cause increased metal loads to water- patterns of migration, which include seasonal movement up- sheds. Although mountain streams appear remote from indus- stream and downstream within a watershed [9]. Resident and trialization and urbanization, many still contain signi®cant altitudinal migrants shared common wintering grounds on the concentrations of heavy metals from natural and anthropogenic river, but most migrants moved upstream onto higher elevation sources [5]. With concerns over environmental impacts of met- creeks in the spring while residents remained on the river to als to freshwater ecosystems, it is important to be able to breed. Eggs of resident dippers had higher levels of mercury monitor the degree of metal exposure to organisms occupying and chlorinated hydrocarbons relative to creek migrants as a mountain streams. result of higher cumulative downstream loadings and differ- The American dipper (Cinclus mexicanus) is a potentially ences in the proportion of ®sh and invertebrates in the diet useful biomonitor of stream pollution because it is a year-round [10]. Dipper diets consisted of 0 to 71% ®sh, with river res- resident of freshwater streams and has an exclusively aquatic idents consuming signi®cantly more ®sh (42%) compared to diet comprised of benthic macroinvertebrates, small ®sh, and creek migrants (22%) [10]. Therefore, we hypothesized that ®sh eggs. Many invertebrate taxa have the ability to bioac- trace-metal concentrations in feathers and feces of resident and cumulate metals to high concentrations without inherent tox- migrant American dippers also may re¯ect the birds' migratory icity to the host species [6]. Freshwater ®sh also can bioac- status or speci®c diet. cumulate organometallic compounds, particularly methylmer- Our main objective was to determine if any differences exist cury (MeHg) due to the high assimilation ef®ciency and the in metal exposure for resident dippers occupying the main river slow elimination rates of this compound [7]. Therefore, pred- and migrant dippers breeding on watershed tributaries using ators feeding on metal- contaminated biota, including the dip- feathers and feces as bioindicators. We further attempted to per, are at risk for elevated exposure from its aquatic diet. identify the major sources of metal contamination to resident Strom et al. [8] con®rmed adult and nestling American dippers and migrant dippers via their ®sh and invertebrate diet. This were exposed to lead through their invertebrate prey in a mine- permitted us to quantify the magnitude of exposure from the impacted river system. Therefore, dippers can be an effective major prey groups and potentially relate it to levels observed in feathers. Although some elements biologically are essential, * To whom correspondence may be addressed all are toxic at high enough concentrations, with some having ([email protected]). a very narrow window of essentiality and toxicity [11]. Thus, 836 Trace-metal exposure to American dippers Environ. Toxicol. Chem. 24, 2005 837 Fig. 1. Map of the study area: The Chilliwack River watershed located near the Canadian±U.S. border in southwestern British Columbia, Canada. in the interest of using the dipper as a biomonitor, we also chinook salmon (;20%) also were included. All samples were modeled the potential toxicological risks of metal exposure to collected during the dipper breeding season before the spring a dipper population with different migratory strategies and freshet over a one-week period in late April 2000 and repeated diets. again in 2001. Samples subsequently were washed three times with distilled deionized water to remove any surface contam- MATERIALS AND METHODS ination or stream water and then transferred and stored frozen Collection of samples in acid-rinsed glass vials until preparation for trace-metal anal- ysis. Samples were collected from the Chilliwack River water- Several breast feathers were removed from individual after- shed (498109N, 1218040W), located in the Cascade Mountains hatch-year dippers at the time of capture and banding for metal in southwestern British Columbia, Canada (Fig. 1). The wa- analysis. Contour (body) feathers are known to have low var- tershed drains an area of 1,274 km2 with elevation ranges from iability and should provide a good measure of individual metal near sea level to over 2,000 m at several mountain peaks. levels across samples [12]. Individual dippers were sexed at Composite samples of benthic invertebrates and salmon fry the time of capture using wing chord measurements [13]. were collected at eight different sites spaced at 4- to 5-km Through the use of color banding, only birds of known mi- intervals along the main stem of the Chilliwack River. Ad- gratory status (river resident or creek migrant) were used for ditional composite samples of invertebrates were collected the metal analysis. We made the assumption that the majority from seven different tributaries in the watershed. Aquatic lar- of birds molted on their breeding site and that feather metal ; val invertebrates ( 1-g dry wt) were collected either by kick pro®les would be indicative of the contaminants accumulated sampling in the stream (disturbing the rocks directly upstream primarily at that site in the preceding year [10]. Each individual of a Surber sampler) or by turning over rocks by hand. The sample of seven to 10 feathers (average mass 5 13 6 4 mg) sample represented a mixture of insect taxa that dippers nat- was stored in polyethylene bags and refrigerated until analyses. urally would prey upon, including approximately equal pro- We used 104 adult feather samples for Hg analysis and 82 of portions of ephemeropteran, plecopteran, and tricopteran lar- these also were analyzed for additional multiple elements. Fe- vae in addition to a much smaller fraction by mass of cole- cal samples (n 5 14) were collected from nestlings (n 5 5) opteran and dipteran larvae. Up to 10 individual salmon fry opportunistically during banding of chicks at 12 to 14 d of (Oncorhynchus spp.) (age 01) that each weighed 100 to 200 age or by following adults (n 5 9) and collecting fresh feces mg fresh weight, were captured live from the Chilliwack River off rocks, with care taken to avoid contamination from the using a dip net and represented a composite sample of pre- substrate. Fecal samples were stored frozen in acid-washed dominantly coho and chum salmon fry (;80%), but pink and plastic containers until analysis. 838 Environ. Toxicol. Chem. 24, 2005 C.A. Morrissey et al. Sample preparation and metal analysis only reported as means of all samples. Pearson product mo- Methods for sample preparation and digestion were adapted ment correlation coef®cients (r) were used to test for corre- and modi®ed from Canadian Wildlife Service method MET- lations among metal concentrations in both feathers and feces. t CHEM-AA-02 [14] and U.S. Environmental Protection Agen- Statistical tests were performed using JMP IN Version 4.0 cy method 200.3 [15]. Feathers were washed with pure ace- (SAS Institute, Cary NC, USA) and the signi®cance level was a5 tone, 1% Triton-X solution alternated with several rinses of set at 0.05.
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