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Metal levels in regrown feathers: Assessment of contamination on the wintering and breeding grounds in the same individuals a
b
Joanna Burger , Ian C. T. Nisbet & Michael Gochfeld
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a
Department of Biological Sciences and Environmental and Occupational Health Sciences Institute (EOHSI) , Rutgers University , P.O. Box 1059, Nelson Hall, Piscataway, New Jersey, 08855 b
I. C. T. Nisbet & Company , Lincoln, Massachusetts
c
Environmental and Community Medicine and EOHSI , UMDNJ, Robert Wood Johnson Medical School , Piscataway, New Jersey Published online: 15 Oct 2009.
To cite this article: Joanna Burger , Ian C. T. Nisbet & Michael Gochfeld (1992) Metal levels in regrown feathers: Assessment of contamination on the wintering and breeding grounds in the same individuals, Journal of Toxicology and Environmental Health: Current Issues, 37:3, 363-374, DOI: 10.1080/15287399209531677 To link to this article: http://dx.doi.org/10.1080/15287399209531677
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METAL LEVELS IN REGROWN FEATHERS: ASSESSMENT OF CONTAMINATION O N THE WINTERING AND BREEDING GROUNDS IN THE SAME INDIVIDUALS Joanna Burger Department of Biological Sciences and Environmental and Occupational Health Sciences Institute (EOHSI), Rutgers University, Piscataway, New Jersey Downloaded by [University of Arizona] at 04:20 19 April 2015
Ian C. T. Nisbet
I. C. T. Nisbet & Company, Lincoln, Massachusetts Michael Gochfeld
Environmental and Community Medicine and EOHSI, UMDNJRobert Wood Johnson Medical School, Piscataway, New Jersey
Birds are useful indicators of environmental contamination because they are relatively large, conspicuous, top predators in food chains. However, concentrations of contaminants in a bird's tissues reflect the bird's exposure over wide temporal and spatial scales. Birds are most useful as monitors of exposure when these scales are known. In this paper we report concentrations of lead, cadmium, mercury, and selenium in breast feathers of common terns (Sterna hirundo) and roseate terns (S. dougallii) trapped during incubation at breeding colonies in New York and Massachusetts. Terns arrived on the breeding grounds with breast feathers grown on their wintering grounds, and regrew certain feathers that were plucked for analysis. The regrown feathers were themselves plucked, and both sets of feathers were analyzed. For roseate terns at Cedar Beach and common terns at both sites there was a significant increase in mercury levels in the feathers grown on the breeding grounds compared to those grown on the wintering ground. The differences in mercury were far greater at Bird Island than at Cedar Beach. Selenium levels at Cedar Beach were higher for the regrown feathers than the initial feathers for roseate terns, but not for common terns. Lead and cadmium levels were not significantly different at either site for either species. These results suggest that terns are exposed to significantly higher levels of mercury in the northeastern United States than they are in the wintering grounds in South America.
We thank the U.S. Fish and Wildlife Service, the New York Department of Environment Conservation, and the Massachusetts Division of Fisheries and Wildlife for permits to collect tern feathers, and the towns of Marion (Bird Island) and Babylon (Cedar Beach) for permission to work in the colonies. This project was partially funded by NIEHS grant (ESO 5022) to EOSHI of Rutgers University and UMDNJ—Robert Wood Johnson Medical School, and by cooperative agreements from the U.S. Fish and Wildlife Service. We thank J. Spendelow for his help throughout the project. We also thank G. Kuhne, J. J. Hatch, T. Plantier, and K. Rio for field assistance, and T. Shukla and T. Benson for laboratory assistance. Requests for reprints should be sent to J. Burger, P.O. Box 1059, Nelson Hall, Rutgers University, Piscataway, NJ 08855.
363 Journal of Toxicology and Environmental Health, 37:363-374, 1992 Copyright © 1992 by Hemisphere Publishing Corporation
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INTRODUCTION Marine and estuarine organisms are exposed to a variety of toxic substances that enter the water from surface runoff, underground leachate, airborne deposition, mobilization from sediments, and migration from bays and estuaries. These organisms can be used as bioindicators or exposure monitors of environmental pollution, and as surrogates for human exposure. Ideally a bioindicator should be sensitive to environmental changes, indicative of the area of interest, and high enough on the food chain to represent the ecosystem of which it is part (Burger, 1989,1992; Mineau et al., 1984; Walsh, 1990). Seabirds are ideal exposure monitors because they are high on the food chain, are sensitive to environmental change, and have successfully provided early warnings of adverse toxic effects. For example, seabirds have been used to monitor local and regional patterns of contamination with petroleum products, organochlorine compounds, metals, and plastics (Nisbet, 1992). In some cases, observations of adverse effects on seabirds have provided early warning of pollution problems (Gilbertson et al., 1991; Koeman, 1972; Ratcliffe, 1967; Risebrough et al., 1971). Our results could bear on the popular belief that pollutants are controlled and regulated in the United States and are uncontrolled and prevalent in South America. Like other exposure monitors, birds accumulate persistent contaminants in their tissues and integrate their exposure over time scales that are determined by the pharmacokinetics of the compounds and over spatial scales that are determined by the movements of the birds. Wideranging or migratory birds may be difficult to use as monitors because it is usually difficult to determine where their exposures occurred. However, this can be turned to advantage by using body feathers as the indicator tissue. Feathers reflect metal levels at the time of their formation when their blood supply is intact (Goede and de Bruin, 1984). Indeed, one mechanism birds have to eliminate heavy metals from their bodies is to sequester them in their feathers (Braune and Gaskin, 1987a, 1987b). For some metals (i.e., mercury) the bird's plumage may account for 93% of the body burden while accounting for only 12% of the body mass (Braune and Gaskin, 1987a). In experimentally exposed gulls, 49% of the dose of mercury is found in the plumage (Lewis and Furness, 1991). Further, levels of certain metals in feathers are highly correlated with levels in other tissues (Gochfeld, 1980; Heinz, 1980). Because of the energetic cost, most birds time their molt so that it does not coincide with breeding or migration (Payne, 1972). Terns (Sterna spp.) replace their body feathers twice each year: once in autumn (before and after migration) and once in spring (before migration; Cramp, 1985). Hence the birds arrive on the breeding grounds with new feathers,
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which have been grown in winter quarters. Metal levels in these feathers reflect the birds' exposure during the winter, as well as any circulating level reflecting the body burden accumulated over a lifetime and mobilized during periods of stress. In this paper we examine the levels of lead, cadmium, mercury, and selenium in the breast feathers of adult common (Sterna hirundo) and roseate (S. dougallii) terns that had recently arrived on the breeding grounds. When breast feathers were pulled from terns, new feathers grew back within 3-4 wk. The same individual birds were retrapped and the regrown feathers were plucked. The regrown feathers contained contaminants acquired by the adult in the period since the previous molt, including the period of 30-50 d since the bird arrived on the breeding grounds. This procedure provides a method for examining metal levels and exposure of the same individuals on the wintering ground and on the breeding ground. Although using the feathers of young birds as indicators of exposure eliminates problems associated with the effects of body burden found in adults, the method of using adults proposed in this paper has several advantages: (1) It provides a yearly estimate of exposure for breeding adults that may be useful for management decisions, and (2) adults may be eating larger fish or different species of fish that have higher concentrations of toxins than the fish they feed their young. Further, we compare metals levels in common terns breeding on Long Island, N.Y., with those breeding in coastal Massachusetts. An examination of high metal levels in sediments reported in the NOAA National Status and Trends report (O'Conner and Ehler, 1991) indicates that the New York estuary ranks highest in the nation for 10 metals and 4 classes of organic pollutants, and that Massachusetts ranks second. MATERIALS AND METHODS
Under appropriate federal and state permits we trapped common and roseate terns at Cedar Beach, Long Island, N.Y., and common terns at Bird Island, Mass., in 1991. Both colonies contain a mixed-species colony of roseate and common terns; colony descriptions can be found in Burger and Gochfeld (1988) and Nisbet et al. (1990). Terns were trapped at the peak and late peak of breeding in the colony, and were banded for individual identification. Common terns were trapped at the beginning of incubation with treadle traps (Burger and Gochfeld, 1991a). Roseate terns were either inadvertently trapped early in incubation, or were trapped at hatching, lost their chicks when they were a few days old, and subsequently relaid eggs at a new nest site (where they were retrapped). About 20 breast feathers were removed from each side under the bend of the wing. This leaves a bare patch similar to the brood patches
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that the birds develop for incubation. On the birds trapped at Bird Island, the feathers surrounding the bare patch were dyed with picric acid in ethanol. Three weeks later we retrapped the same individuals and collected the regrown feathers. These could readily be identified (1) by their partial sheaths, (2) by being whiter (common tern) or brighter pink (roseate tern) than the surrounding feathers, and (3) at Bird Island, by being surrounded by dyed feathers. Our procedures did not result in any desertions by either species. One potential source of bias is that in 3 weeks the new feathers are not completely regrown, and they retain some blood supply in the base of the feathers. It was not practicable to collect fully regrown feathers because the birds cannot be trapped after the chicks hatch. To determine if the blood remaining in the feather shaft could bias our analysis, we collected feathers from 14 other common tern chicks recently killed by cats. We compared the metal levels in the partially formed wing feathers (with blood supply) with fully formed breast feathers in the same chicks. Preparation, extraction, and analytical methods were modified from U.S. Environmental Protection Agency (EPA) procedures (EPA, 1981). Feathers were washed vigorously in deionized water alternated with acetone to remove loosely adherent external contamination, were digested in warm nitric acid with the addition of 50% hydrogen peroxide, and were subsequently diluted in deionized water. Mercury was analyzed by the cold vapor technique, and the other metals were analyzed by graphite furnace atomic absorption (Perkin-Elmer 6500). All concentrations are expressed in ppb (ng g" ) on a dry weight basis using weights obtained from air-dried specimens. Detection limits ranged from 0.3 ppb for cadmium to about 10 ppb for lead. All specimens were run in batches that included a standard calibration curve, a standard from the National Bureau of Standards, and spiked specimens. The recoveries ranged from 78 to 112%, and only batches with recovery >85% were used. Concentrations reported were not corrected for incomplete recovery. The coefficient of variation on replicate, spiked samples ranged from 2 to 4%. We used the SAS Kruskal-Wallis x2 test to compare levels among species (SAS Institute, Inc., 1985). Differences between original and regrown feathers were compared overall with Kruskal-Wallis x tests, and within the same individuals with paired f-tests. RESULTS Initial and Regrown Feathers
There were no significant changes in levels of lead or cadmium in the initial and regrown feathers in either roseate and common terns nesting at Cedar Beach or Bird Island (Table 1). Selenium levels did not change significantly in common terns, but increased significantly (by a factor of 3.5) in roseate terns at Cedar Beach.
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TABLE T. Metal Levels in Feathers of Common and Roseate Ternsa
Species
Location
Stage
Number
Common tern
Cedar Beach
Initial Regrown
15 15
Initial Regrown
7 7
Initial Regrown
8 8
Kruskal-Wallis x 2 (p) Paired i-test (p) Bird Island Kruskal-Wallis x 2 (p) Paired f-test (p) Roseate tern
Cedar Beach Kruskal-Wallis x 2 (p) Paired t-test (p)
Lead
Cadmium
Mercury
Selenium
3600 ± 760(2800) 3600 ± 1100 (2300) 0.5 (NS) 0.1 (NS) 1500 ± 560(1100) 100 ± 340(750) 0.2 (NS) 0.5 (NS)
150 ± 37(110) 120 ± 30 (88) 0.9 (NS) 0.7 (NS) 120 ± 47(80) 420 ± 310 (130) 0.8 (NS) 0.9 (NS)
5000 ± 1100 (2900) 8300 ± 1100 (7400) 5.1 (.02) 1.7 (.06) 1800 ± 1200 (530) 11,800 ± 1468 (11,418) 2.4 (.007) 9.8 (.0002)
2900 ± 300 (2600) 2100 ± 190 (1900) 1.7 (NS) 1.7 (NS) 1100 ± 120 (1000) 2000 ± 420 (1500) 2.5 (NS) 2.1 (.08)
1030 ± 340 (720) 1500 ± 460(1300) 2.1 (NS) 0.8 (NS)
85 ± 14(77) 160 ± 34 3.1 (.07) 2.2 (.06)
2700 ± 970(2100) 7500 ± 1200 (6400) 4.3 (.03) 2.1 (.07)
1100 ± 130 (1000) 3900 ± 860 (3300) 9.2 (.002) 3.3 (.01)
Note. Shown are mean ± SE for arithmetic means (geometric means) in ppb dry weight rounded to two significant figures.
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Mercury levels, however, were significantly higher in the regrown feathers compared to the feathers collected initially in all three samples (Table 1). Mercury levels (geometric means) at Cedar Beach increased by a factor of 2.5, while at Bird Island they increased by a factor of 21.5. Geographic and Species Differences There were significant species and geographic differences (Table 2). Levels of lead, mercury, and selenium were significantly higher in the common terns from Cedar Beach than from Bird Island in the initial collection, but in the regrown feathers only lead differed significantly with higher levels at Cedar Beach than Bird Island (Table 2). We then compared the common and roseate terns at Cedar Beach (Table 2). Lead and selenium levels were significantly higher in common terns compared to roseate terns in the initial collection, but in the regrown feathers roseate terns had significantly higher levels than the common terns. DISCUSSION Methodological Considerations Feathers are ideal for exposure monitoring or biomonitoring of metals because they can be sampled noninvasively with minimal stress to the bird, they can be stored easily without refrigeration, they regrow relatively quickly, and they sequester many metals (Goede and de Bruin, 1984; Burger and Gochfeld, 1991b). Our procedure of sampling feathers twice from the same individual birds permits comparison of feathers grown at different times and in different places, reflecting the birds' exposure in different areas. We found it easy to identify the regrown feathers using the three criteria given under Materials and Methods. Logistic difficulties in trapTABLE 2. Comparisons of Metal Levels Among Species and Locations Species
Comparison
Lead
Cadmium
Mercury
Selenium
Common tern with common tern
Initial collection, Cedar Beach with Bird Island Regrown collection, Cedar Beach with Bird Island Initial collection at Cedar Beach Regrown collection at Cedar Beach
5.5 (.01)
0.7 (NS)
4.7 (.03)
12.2 (0.005)
5.4 (.02)
0.3 (NS)
2.5 (NS)
0.0 (NS)
8.4 (.005)
1.2 (NS)
1.7 (NS)
13.5 (.0005)
1.2 (NS)
2.0 (NS)
2.0 (NS)
4.8 (.05)
Roseate tern with common tern
Note. Given are Kruskal-Wallis x 2 (probability levels).
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ping individual birds at the beginning and end of incubation, and in keeping track of these individuals to trap them on the appropriate days, as well as the necessity to minimize disturbance of the endangered roseate tern, led to relatively small sample sizes for roseate terns at Cedar Beach and for common terns at Bird Island. However, the sample size for common terns at Cedar Beach was adequate, and the similarity of our results across species and locations adds strength to the findings. The major methodological issue raised in our study is whether the "regrown" feathers, which were incompletely grown on the latest dates when they could be collected, were fully comparable with the old feathers. The distal end (vanes) of the regrown feathers should be directly comparable to the complete old feathers. Results from a comparison of fully formed breast feathers with the proximal end of partially formed wing feathers suggests that partially formed feathers (including the blood-filled sheath) contained similar concentrations of cadmium and selenium to those fully formed, but lower concentrations of lead and mercury. The ratio for partially developed to fully formed feathers was 1 :1.53 for lead and 1 :1.30 for mercury (J- Burger and M. Gochfeld, unpublished results). Thus, inclusion of partially formed feathers in the analysis may have led to some downward bias in the reported concentrations of lead and mercury, although not by more than 33 and 23% respectively. This bias would have led to understatement of the magnitude of the increase in mercury concentrations between the initial and regrown feathers. For example, if it is assumed that the mercury concentrations in the regrown feathers of common terns at Cedar Beach were biased downwards by 23%, the corrected value of the geometric mean would have been 9.6 /¿g g" 1 , representing an increase by a factor of 3.3 instead of the factor of 2.6 shown in Table 1. It is unlikely that this bias would have obscured a significant increase in lead concentrations, except perhaps in the roseate terns at Cedar Beach. Differential Temporal Exposure
Feathers are useful indicators of exposure to metals in birds because they reflect the levels of the metals circulating in the blood at the time when the feather was growing (Braune and Gaskin, 1987a, 1987b). However, circulating levels of metals in the blood are derived not only from current exposure, but also by mobilization from various organs in which the metals are stored (Osborn, 1979). Once feather growth is completed, the blood supply atrophies, the feathers become physiologically isolated from other tissues, and their metal content is extremely resistant to further change under the influence of heat, light or other forms of weathering, with very little evidence for contamination under field conditions (Applequist et al., 1984; Goede and de Bruin, 1984; Walsh, 1990). Further, the pooling of a number of small body feathers can minimize variations
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in the concentrations of metals in feathers dependent on the stage of molt (Furness et al., 1986). In our study, there were no significant changes in lead and cadmium concentrations in the regrown versus the initial feathers, but there were significant increases in mercury levels in both species of tern, and in selenium levels in roseate terns. These data clearly indicate that exposure to mercury on the breeding grounds was much higher than that on the wintering grounds. Mercury levels in common terns increased by a factor of about 3 at Cedar Beach, and by a factor of about 21 at Bird Island. Mercury levels in feathers of roseate terns at Cedar Beach increased by a factor of about 3, similar to that in common terns at the same site. Any bias resulting from the use of incompletely grown feathers would have led to underestimation of these differences, as discussed above. Several studies have shown that feathers are a major excretory pathway for mercury in seabirds, including gulls and terns (Braune, 1987; Braune and Gaskin, 1987a, 1987b; Furness et al., 1986, 1990). In Bonaparte's gulls (Larus Philadelphia), the total content of Hg in the body (excluding the feathers) declined by 88% during the period of autumn molt. Redistribution of mercury into the growing feathers accounted for about 64% of gross losses, and 106% of net losses, from the body during this period (Braune and Gaskin, 1987b). After the molt, feathers included about 93% of the total load of mercury carried by the birds (Braune and Gaskin, 1987a). In red-billed gulls (L novaehollandiae), mercury concentrations in feathers did not increase with age (Furness et al., 1990), indicating that most or all of the mercury accumulated in the body is eliminated with each molt. Although data on terns are limited (Braune, 1987), terns are closely related to gulls and would be expected to be similar in these toxicokinetic characteristics. Hence it would be expected that mercury concentrations in the initial feather collections would reflect the birds' exposure prior to the spring molt (i.e., in the winter quarters between October and April), whereas mercury concentrations in the regrown feathers would reflect the birds' exposure between the spring molt and the time of collection in June. Only part of this exposure would have taken place on the breeding grounds, and it is unlikely that the birds' body burdens would have reached steady state within the 30-50 days after arrival there. Hence, the 3- to 21-fold increases in mercury concentrations observed between the initial and regrown feather collections would not fully reflect the differences in exposure. No data appear to have been published on the importance of feathers as a route of excretion of lead, cadmium, or selenium in seabirds. It is possible that some of the body burdens may be retained through each molt. Hence, it is not clear that the differences between concentrations of these metals in the initial and regrown feathers would accurately reflect differences in exposure. Although the significant increase in sele-
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nium levels in roseate terns (Table 1) presumably indicates an increase in exposure, the magnitude of this increase may be understated, and other significant changes could have been missed. Overall, our data indicate that both species are much more highly exposed to mercury, roseate terns are more highly exposed to selenium, and both species may be more highly exposed to cadmium on their breeding grounds than in their winter quarters. These results probably reflect the fact that both breeding locations are in the industrial northeastern United States, where concentrations of these metals in marine sediments are elevated (O'Conner and Ehler, 1991). Differences Between Locations In the initial collections of common tern feathers, concentrations of lead, mercury, and cadmium were significantly higher at Cedar Beach than at Bird Island (Table 2). The main winter quarters of common terns are in eastern South America, from Trinidad to southern Brazil (Austin, 1953). Banding data suggest that common terns from colonies in New York and Massachusetts, including Cedar Beach and Bird Island, overlap widely or completely in autumn migration and in winter quarters (Austin, 1953; unpublished data of the authors). Hence, we would not have predicted differences in the initial concentrations. In the case of lead, there was a similar difference in concentrations in the regrown feathers (Table 2), so the differences in the initial collection could have resulted from carryover of residues accumulated during the previous summer. This explanation, however, cannot account for the intercolony differences in levels of mercury and selenium. These differences suggest that common terns from these colonies may be differentially exposed to mercury and selenium in the winter quarters. This suggests that the birds from these colonies may be segregated in the winter quarters, either geographically or ecologically, possibilities that require investigation. In the regrown feathers, concentrations of lead were significantly higher at Cedar Beach. Some of the levels of these metals in both species of terns were notably high in relation to other data on inshore seabirds. Although both breeding sites are located in polluted regions (O'Conner and Ehler, 1991), there is little information to associate the exposures with specific local sources. At Cedar Beach, both species of tern feed mainly within 10 km of the colony (Safina, 1990), an area characterized by suburban and recreational development with no known major sources of metal pollution except for heavy automobile traffic and industrialized areas (New York City, northern New jersey) 100-200 km to the west and southwest. At Bird Island, common terns feed mainly within 20 km of the colony in Buzzards Bay (including a few birds in New Bedford Harbor) and Vineyard Sound (Nisbet, 1981, 1983, and unpublished observations; D. Heinemann, personal communication). New Bedford Harbor is highly polluted with lead and cadmium, among other pollutants (Genest and
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Hatch, 1981; Sears and Battaglia, 1990, Summerhayes et al., 1977), which may explain the high concentrations of cadmium in a few of the birds from Bird Island (Table 1). However, there is little evidence that New Bedford is a major source of mercury, and the highest concentration of mercury found in sediment in a recent survey of Buzzards Bay was only 0.4 /tg g" 1 (Sears and Battaglia, 1990). This would not account for the strikingly and uniformly high levels of mercury in the regrown feathers of common terns at Bird Island (Table 1). Further investigation of the sources of mercury in the terns at Bird Island is needed.
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Differences Between Species
The species difference at Cedar Beach is interesting because both species feed in the same general area on the same species of fish during the breeding season (Safina, 1990), although roseates take smaller individuals. Roseate terns had significantly lower lead and selenium levels in their breast feathers when they arrived on the breeding grounds than common terns. However, levels in regrown feathers for the birds feeding near Cedar Beach were not significantly different with respect to species (except for selenium). This suggests that roseate and common terns at Cedar Beach are exposed to similar levels of these metals in their food, and that species differences primarily reflect exposure on the wintering ground. Overall, the levels and patterns of occurrence of metals in initial and regrown feathers suggest that initial species and locational differences may be due to differences in exposure on the wintering grounds, and that their exposure on the breeding grounds may be equal to (or much greater than, in the case of mercury) their exposure on the wintering grounds. REFERENCES Applequist, H., Asbirk, S., and Draback, L. 1984. Mercury monitoring: Mercury stability in bird feathers. Mar. Pollut. Bull. 15:22-27. Austin, O. L., Sr. 1953. The migration of the common tern (Sterna hirundo) in the Western Hemisphere. Bird-Banding 24:39-55. Braune, B. M. 1987. Comparison of total mercury levels in relation to diet and molt for nine species of marine birds. Arch. Environ. Toxicol. Contam. 16:217-224. Braune, B. M., and Gaskin, D. E. 1987a. Mercury levels in Bonaparte's gull (Larus Philadelphia) during autumn molt in the Quoddy region, New Brunswick, Canada. Arch. Environ. Contam. Toxicol. 16:539-549. Braune, B. M., and Gaskin, D. E. 1987b. A mercury budget for the Bonaparte's gull during autumn moult. Ornis Scand. 18:244-250. Burger, J. 1989. Least tern populations in coastal New Jersey: Monitoring and managing of a regionally endangered species. J. Coastal Research 5:801-811. Burger, J. 1992. Ecological effects of exposure to hazardous waste sites. In Evaluation and Management of Hazardous Waste, eds. J. A. Moore, B. V. Subramanyam and R. G. Tardiff. London: Wiley, in press.
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Burger, J., and Gochfeld, M. 1988. Nest site selection and temporal patterns in habitat use of roseate and common terns. Auk 105:433-438. Burger, J., and Gochfeld, M. 1991a. Reproductive vulnerability; parental attendance around hatching in roseate (Sterna dougallii) and common (S. hirudo) terns. Condor 93:125-129. Burger, J., and Gochfeld, M. 1991b. Lead, mercury, and cadmium in feathers of tropical terns in Puerto Rico and Australia. Arch. Environ. Contarn. Toxicol. 21:311-315. Cramp, S. 1985. Handbook of the Birds of Europe, the Middle East, and North Africa, vol. IV. Oxford: Oxford University Press. Environmental Protection Agency. 1981. Interim methods for sampling and analysis of priority pollutants in sediments and fish tissues. U.S. Environmental Protection Agency, EPA 600/4-81055, Cincinnati. Furness, R. W., Muirhead, S. J., and Woodburn, M. 1986. Using bird feathers to measure mercury in the environment: Relationships between mercury content and moult. Mar. Pollut. Bull. 17:27-37. Furness, R. W., Lewis, S. A., and Mills, J. A. 1990. Mercury levels in the plumage of red-billed gulls Laws novaehollandiae scopulinus of known sex and age. Environ. Pollut. 63:33-39. Genest, P. E., and Hatch, W. I. 1981. Heavy metals in Mercenaria mercenaria and sediments from the New Bedford Harbor region of Buzzards Bay, North Atlantic. Bull. Environ. Contam. Toxicol. 26:124-130. Gilbertson, M., Kubiak, T., Ludwig, J., and Fox, G. 1991. Great Lakes embryo mortality, edema, and deformities syndrome (GLEMEDS) in colonial fish-eating birds: Similarity to chick-edema disease. J. Toxicol. Environ. Health 33:455-520. Gochfeld, M. 1980. Tissue distribution of mercury in normal and abnormal young common terns. Mar. Pollut. Bull. 11:362-366. Goede, A. A., and de Bruin, M. 1984. The use of bird feather parts as a monitor for metal pollution. Environ. Pollut. Ser. B. 8:281-298. Heinz, G. H. 1980. Comparison of game-farm and wild-strain mallard ducks in accumulation of methylmercury. J. Environ. Pathol. Toxicol. 3:379-386. Koeman, J. H., ed. 1972. Side-effects of persistent pesticides and other chemicals on birds and mammals in the Netherlands. TNO-Nieuws 27:527-632. Lewis, S.A., and Furness, R. W. 1991. Mercury accumulation and excretion in laboratory reared black-headed gull Larus ridibundus chicks. Arch. Environ. Contam. Toxicol. 21:316-320. Mineau, P., Fox, G. A., Norstrom, R. J., Weseloh, D. V., Hallett, D. J., and Ellenton, J. A. 1984. Using the herring gull to monitor levels and effects of organochlorine contamination in the Canadian Great Lakes. In Toxic Contaminants in the Great Lakes, eds. J. O. Nriagu and M. S. Simmons, pp. 426-451. New York: Wiley. Nisbet, I. C. T. 1981. Behavior of common and roseate terns after trapping. Colonial Waterbirds 4:44-46. Nisbet, I. C. T. 1983. Territorial feeding by common terns. Colonial Waterbirds 6:64-70. Nisbet, I. C. T. 1992. Effects of pollution on marine birds. In Seabirds on Islands: Threats, Case Studies and Action Plans, eds. D. N. Nettleship, J. Burger, and M. Gochfeld. ICBP Tech. Publ. Cambridge, U.K.: International Council on Bird Preservation, in press. Nisbet, I. C. T., Burger, J., Gochfeld, M., and Safina, C. 1990. Estimating fledging success and productivity in roseate terns (Sterna dougallii). Colonial Waterbirds 13:85-91. O'Conner, T. P., and Ehler, C. N. 1991. Results from the NOAA National Status and Trends program on distribution and effects of chemical contamination in the coastal and estuarine United States. Environ. Monit. Assess. 17:33-49. Osborn, P. 1979. Seasonal changes in the fat, protein and metal content of the liver of starling Sturnus vulgaris. Environ. Pollut. 19:145-155. Payne, R. B. 1972. Mechanisms and control of molt. In Avian Biology, vol. 2, eds. D. S. Farner and J. R. King, Chapter 3. New York: Academic Press. Ratcliffe, D. A. 1967. Decrease in eggshell weight of certain birds of prey. Nature 215:208-210. Risebrough, R. W. 1986. Pesticides and bird populations. Curr. Ornithol. 3:397-427.
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Risebrough, R. W., Sibley, F. C., and Kirven, M. N. 1971. Reproductive failure of the brown pelican on Anacapa Island in 1969. Am. Birds 25:8-9. Safina, C. 1990. Foraging habitat partitioning in roseate and common terns. Auk 107:351-358. SAS Institute, Inc. 1985. SAS User's Guide, 1985 Edition. Cary, N.C.: SAS Institute, Inc. Sears, J. R., and Battaglia, J. 1990. Use of benthic seaweeds to monitor heavy metals in Buzzards Bay, adjacent estuaries and New Bedford Harbor, Massachusetts. Technical Report 87-10 to Massachusetts Department of Environmental Protection. Southern Massachusetts University, North Dartmouth, Mass. Summerhayes, C. P., Ellis, J. P., Stoffers, P., Briggs, S. R., and Fitzgerald, M. G. 1977. Fine-grained sediment and industrial waste distribution and dispersal in New Bedford Harbor and western Buzzards Bay, Massachusetts. Woods Hole Oceanographic Institute Tech. Rep. WHOI-76-115, Woods Hole, Mass. Walsh, P. M. 1990. The use of seabirds as monitors of heavy metals in the marine environment. In Heavy Metals in the Marine Environment, eds. R. W. Furness and P. S. Rainbow, pp. 183-204. Boca Raton, Fla.: CRC Press. Received February 17, 1992 Accepted June 9, 1992
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Metal levels in regrown feathers: Assessment of contamination on the wintering and breeding grounds in the same individuals a
b
Joanna Burger , Ian C. T. Nisbet & Michael Gochfeld
c
a
Department of Biological Sciences and Environmental and Occupational Health Sciences Institute (EOHSI) , Rutgers University , P.O. Box 1059, Nelson Hall, Piscataway, New Jersey, 08855 b
I. C. T. Nisbet & Company , Lincoln, Massachusetts
c
Environmental and Community Medicine and EOHSI , UMDNJ, Robert Wood Johnson Medical School , Piscataway, New Jersey Published online: 15 Oct 2009.
To cite this article: Joanna Burger , Ian C. T. Nisbet & Michael Gochfeld (1992) Metal levels in regrown feathers: Assessment of contamination on the wintering and breeding grounds in the same individuals, Journal of Toxicology and Environmental Health: Current Issues, 37:3, 363-374, DOI: 10.1080/15287399209531677 To link to this article: http://dx.doi.org/10.1080/15287399209531677
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METAL LEVELS IN REGROWN FEATHERS: ASSESSMENT OF CONTAMINATION O N THE WINTERING AND BREEDING GROUNDS IN THE SAME INDIVIDUALS Joanna Burger Department of Biological Sciences and Environmental and Occupational Health Sciences Institute (EOHSI), Rutgers University, Piscataway, New Jersey Downloaded by [University of Arizona] at 04:20 19 April 2015
Ian C. T. Nisbet
I. C. T. Nisbet & Company, Lincoln, Massachusetts Michael Gochfeld
Environmental and Community Medicine and EOHSI, UMDNJRobert Wood Johnson Medical School, Piscataway, New Jersey
Birds are useful indicators of environmental contamination because they are relatively large, conspicuous, top predators in food chains. However, concentrations of contaminants in a bird's tissues reflect the bird's exposure over wide temporal and spatial scales. Birds are most useful as monitors of exposure when these scales are known. In this paper we report concentrations of lead, cadmium, mercury, and selenium in breast feathers of common terns (Sterna hirundo) and roseate terns (S. dougallii) trapped during incubation at breeding colonies in New York and Massachusetts. Terns arrived on the breeding grounds with breast feathers grown on their wintering grounds, and regrew certain feathers that were plucked for analysis. The regrown feathers were themselves plucked, and both sets of feathers were analyzed. For roseate terns at Cedar Beach and common terns at both sites there was a significant increase in mercury levels in the feathers grown on the breeding grounds compared to those grown on the wintering ground. The differences in mercury were far greater at Bird Island than at Cedar Beach. Selenium levels at Cedar Beach were higher for the regrown feathers than the initial feathers for roseate terns, but not for common terns. Lead and cadmium levels were not significantly different at either site for either species. These results suggest that terns are exposed to significantly higher levels of mercury in the northeastern United States than they are in the wintering grounds in South America.
We thank the U.S. Fish and Wildlife Service, the New York Department of Environment Conservation, and the Massachusetts Division of Fisheries and Wildlife for permits to collect tern feathers, and the towns of Marion (Bird Island) and Babylon (Cedar Beach) for permission to work in the colonies. This project was partially funded by NIEHS grant (ESO 5022) to EOSHI of Rutgers University and UMDNJ—Robert Wood Johnson Medical School, and by cooperative agreements from the U.S. Fish and Wildlife Service. We thank J. Spendelow for his help throughout the project. We also thank G. Kuhne, J. J. Hatch, T. Plantier, and K. Rio for field assistance, and T. Shukla and T. Benson for laboratory assistance. Requests for reprints should be sent to J. Burger, P.O. Box 1059, Nelson Hall, Rutgers University, Piscataway, NJ 08855.
363 Journal of Toxicology and Environmental Health, 37:363-374, 1992 Copyright © 1992 by Hemisphere Publishing Corporation
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INTRODUCTION Marine and estuarine organisms are exposed to a variety of toxic substances that enter the water from surface runoff, underground leachate, airborne deposition, mobilization from sediments, and migration from bays and estuaries. These organisms can be used as bioindicators or exposure monitors of environmental pollution, and as surrogates for human exposure. Ideally a bioindicator should be sensitive to environmental changes, indicative of the area of interest, and high enough on the food chain to represent the ecosystem of which it is part (Burger, 1989,1992; Mineau et al., 1984; Walsh, 1990). Seabirds are ideal exposure monitors because they are high on the food chain, are sensitive to environmental change, and have successfully provided early warnings of adverse toxic effects. For example, seabirds have been used to monitor local and regional patterns of contamination with petroleum products, organochlorine compounds, metals, and plastics (Nisbet, 1992). In some cases, observations of adverse effects on seabirds have provided early warning of pollution problems (Gilbertson et al., 1991; Koeman, 1972; Ratcliffe, 1967; Risebrough et al., 1971). Our results could bear on the popular belief that pollutants are controlled and regulated in the United States and are uncontrolled and prevalent in South America. Like other exposure monitors, birds accumulate persistent contaminants in their tissues and integrate their exposure over time scales that are determined by the pharmacokinetics of the compounds and over spatial scales that are determined by the movements of the birds. Wideranging or migratory birds may be difficult to use as monitors because it is usually difficult to determine where their exposures occurred. However, this can be turned to advantage by using body feathers as the indicator tissue. Feathers reflect metal levels at the time of their formation when their blood supply is intact (Goede and de Bruin, 1984). Indeed, one mechanism birds have to eliminate heavy metals from their bodies is to sequester them in their feathers (Braune and Gaskin, 1987a, 1987b). For some metals (i.e., mercury) the bird's plumage may account for 93% of the body burden while accounting for only 12% of the body mass (Braune and Gaskin, 1987a). In experimentally exposed gulls, 49% of the dose of mercury is found in the plumage (Lewis and Furness, 1991). Further, levels of certain metals in feathers are highly correlated with levels in other tissues (Gochfeld, 1980; Heinz, 1980). Because of the energetic cost, most birds time their molt so that it does not coincide with breeding or migration (Payne, 1972). Terns (Sterna spp.) replace their body feathers twice each year: once in autumn (before and after migration) and once in spring (before migration; Cramp, 1985). Hence the birds arrive on the breeding grounds with new feathers,
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which have been grown in winter quarters. Metal levels in these feathers reflect the birds' exposure during the winter, as well as any circulating level reflecting the body burden accumulated over a lifetime and mobilized during periods of stress. In this paper we examine the levels of lead, cadmium, mercury, and selenium in the breast feathers of adult common (Sterna hirundo) and roseate (S. dougallii) terns that had recently arrived on the breeding grounds. When breast feathers were pulled from terns, new feathers grew back within 3-4 wk. The same individual birds were retrapped and the regrown feathers were plucked. The regrown feathers contained contaminants acquired by the adult in the period since the previous molt, including the period of 30-50 d since the bird arrived on the breeding grounds. This procedure provides a method for examining metal levels and exposure of the same individuals on the wintering ground and on the breeding ground. Although using the feathers of young birds as indicators of exposure eliminates problems associated with the effects of body burden found in adults, the method of using adults proposed in this paper has several advantages: (1) It provides a yearly estimate of exposure for breeding adults that may be useful for management decisions, and (2) adults may be eating larger fish or different species of fish that have higher concentrations of toxins than the fish they feed their young. Further, we compare metals levels in common terns breeding on Long Island, N.Y., with those breeding in coastal Massachusetts. An examination of high metal levels in sediments reported in the NOAA National Status and Trends report (O'Conner and Ehler, 1991) indicates that the New York estuary ranks highest in the nation for 10 metals and 4 classes of organic pollutants, and that Massachusetts ranks second. MATERIALS AND METHODS
Under appropriate federal and state permits we trapped common and roseate terns at Cedar Beach, Long Island, N.Y., and common terns at Bird Island, Mass., in 1991. Both colonies contain a mixed-species colony of roseate and common terns; colony descriptions can be found in Burger and Gochfeld (1988) and Nisbet et al. (1990). Terns were trapped at the peak and late peak of breeding in the colony, and were banded for individual identification. Common terns were trapped at the beginning of incubation with treadle traps (Burger and Gochfeld, 1991a). Roseate terns were either inadvertently trapped early in incubation, or were trapped at hatching, lost their chicks when they were a few days old, and subsequently relaid eggs at a new nest site (where they were retrapped). About 20 breast feathers were removed from each side under the bend of the wing. This leaves a bare patch similar to the brood patches
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that the birds develop for incubation. On the birds trapped at Bird Island, the feathers surrounding the bare patch were dyed with picric acid in ethanol. Three weeks later we retrapped the same individuals and collected the regrown feathers. These could readily be identified (1) by their partial sheaths, (2) by being whiter (common tern) or brighter pink (roseate tern) than the surrounding feathers, and (3) at Bird Island, by being surrounded by dyed feathers. Our procedures did not result in any desertions by either species. One potential source of bias is that in 3 weeks the new feathers are not completely regrown, and they retain some blood supply in the base of the feathers. It was not practicable to collect fully regrown feathers because the birds cannot be trapped after the chicks hatch. To determine if the blood remaining in the feather shaft could bias our analysis, we collected feathers from 14 other common tern chicks recently killed by cats. We compared the metal levels in the partially formed wing feathers (with blood supply) with fully formed breast feathers in the same chicks. Preparation, extraction, and analytical methods were modified from U.S. Environmental Protection Agency (EPA) procedures (EPA, 1981). Feathers were washed vigorously in deionized water alternated with acetone to remove loosely adherent external contamination, were digested in warm nitric acid with the addition of 50% hydrogen peroxide, and were subsequently diluted in deionized water. Mercury was analyzed by the cold vapor technique, and the other metals were analyzed by graphite furnace atomic absorption (Perkin-Elmer 6500). All concentrations are expressed in ppb (ng g" ) on a dry weight basis using weights obtained from air-dried specimens. Detection limits ranged from 0.3 ppb for cadmium to about 10 ppb for lead. All specimens were run in batches that included a standard calibration curve, a standard from the National Bureau of Standards, and spiked specimens. The recoveries ranged from 78 to 112%, and only batches with recovery >85% were used. Concentrations reported were not corrected for incomplete recovery. The coefficient of variation on replicate, spiked samples ranged from 2 to 4%. We used the SAS Kruskal-Wallis x2 test to compare levels among species (SAS Institute, Inc., 1985). Differences between original and regrown feathers were compared overall with Kruskal-Wallis x tests, and within the same individuals with paired f-tests. RESULTS Initial and Regrown Feathers
There were no significant changes in levels of lead or cadmium in the initial and regrown feathers in either roseate and common terns nesting at Cedar Beach or Bird Island (Table 1). Selenium levels did not change significantly in common terns, but increased significantly (by a factor of 3.5) in roseate terns at Cedar Beach.
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TABLE T. Metal Levels in Feathers of Common and Roseate Ternsa
Species
Location
Stage
Number
Common tern
Cedar Beach
Initial Regrown
15 15
Initial Regrown
7 7
Initial Regrown
8 8
Kruskal-Wallis x 2 (p) Paired i-test (p) Bird Island Kruskal-Wallis x 2 (p) Paired f-test (p) Roseate tern
Cedar Beach Kruskal-Wallis x 2 (p) Paired t-test (p)
Lead
Cadmium
Mercury
Selenium
3600 ± 760(2800) 3600 ± 1100 (2300) 0.5 (NS) 0.1 (NS) 1500 ± 560(1100) 100 ± 340(750) 0.2 (NS) 0.5 (NS)
150 ± 37(110) 120 ± 30 (88) 0.9 (NS) 0.7 (NS) 120 ± 47(80) 420 ± 310 (130) 0.8 (NS) 0.9 (NS)
5000 ± 1100 (2900) 8300 ± 1100 (7400) 5.1 (.02) 1.7 (.06) 1800 ± 1200 (530) 11,800 ± 1468 (11,418) 2.4 (.007) 9.8 (.0002)
2900 ± 300 (2600) 2100 ± 190 (1900) 1.7 (NS) 1.7 (NS) 1100 ± 120 (1000) 2000 ± 420 (1500) 2.5 (NS) 2.1 (.08)
1030 ± 340 (720) 1500 ± 460(1300) 2.1 (NS) 0.8 (NS)
85 ± 14(77) 160 ± 34 3.1 (.07) 2.2 (.06)
2700 ± 970(2100) 7500 ± 1200 (6400) 4.3 (.03) 2.1 (.07)
1100 ± 130 (1000) 3900 ± 860 (3300) 9.2 (.002) 3.3 (.01)
Note. Shown are mean ± SE for arithmetic means (geometric means) in ppb dry weight rounded to two significant figures.
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Mercury levels, however, were significantly higher in the regrown feathers compared to the feathers collected initially in all three samples (Table 1). Mercury levels (geometric means) at Cedar Beach increased by a factor of 2.5, while at Bird Island they increased by a factor of 21.5. Geographic and Species Differences There were significant species and geographic differences (Table 2). Levels of lead, mercury, and selenium were significantly higher in the common terns from Cedar Beach than from Bird Island in the initial collection, but in the regrown feathers only lead differed significantly with higher levels at Cedar Beach than Bird Island (Table 2). We then compared the common and roseate terns at Cedar Beach (Table 2). Lead and selenium levels were significantly higher in common terns compared to roseate terns in the initial collection, but in the regrown feathers roseate terns had significantly higher levels than the common terns. DISCUSSION Methodological Considerations Feathers are ideal for exposure monitoring or biomonitoring of metals because they can be sampled noninvasively with minimal stress to the bird, they can be stored easily without refrigeration, they regrow relatively quickly, and they sequester many metals (Goede and de Bruin, 1984; Burger and Gochfeld, 1991b). Our procedure of sampling feathers twice from the same individual birds permits comparison of feathers grown at different times and in different places, reflecting the birds' exposure in different areas. We found it easy to identify the regrown feathers using the three criteria given under Materials and Methods. Logistic difficulties in trapTABLE 2. Comparisons of Metal Levels Among Species and Locations Species
Comparison
Lead
Cadmium
Mercury
Selenium
Common tern with common tern
Initial collection, Cedar Beach with Bird Island Regrown collection, Cedar Beach with Bird Island Initial collection at Cedar Beach Regrown collection at Cedar Beach
5.5 (.01)
0.7 (NS)
4.7 (.03)
12.2 (0.005)
5.4 (.02)
0.3 (NS)
2.5 (NS)
0.0 (NS)
8.4 (.005)
1.2 (NS)
1.7 (NS)
13.5 (.0005)
1.2 (NS)
2.0 (NS)
2.0 (NS)
4.8 (.05)
Roseate tern with common tern
Note. Given are Kruskal-Wallis x 2 (probability levels).
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ping individual birds at the beginning and end of incubation, and in keeping track of these individuals to trap them on the appropriate days, as well as the necessity to minimize disturbance of the endangered roseate tern, led to relatively small sample sizes for roseate terns at Cedar Beach and for common terns at Bird Island. However, the sample size for common terns at Cedar Beach was adequate, and the similarity of our results across species and locations adds strength to the findings. The major methodological issue raised in our study is whether the "regrown" feathers, which were incompletely grown on the latest dates when they could be collected, were fully comparable with the old feathers. The distal end (vanes) of the regrown feathers should be directly comparable to the complete old feathers. Results from a comparison of fully formed breast feathers with the proximal end of partially formed wing feathers suggests that partially formed feathers (including the blood-filled sheath) contained similar concentrations of cadmium and selenium to those fully formed, but lower concentrations of lead and mercury. The ratio for partially developed to fully formed feathers was 1 :1.53 for lead and 1 :1.30 for mercury (J- Burger and M. Gochfeld, unpublished results). Thus, inclusion of partially formed feathers in the analysis may have led to some downward bias in the reported concentrations of lead and mercury, although not by more than 33 and 23% respectively. This bias would have led to understatement of the magnitude of the increase in mercury concentrations between the initial and regrown feathers. For example, if it is assumed that the mercury concentrations in the regrown feathers of common terns at Cedar Beach were biased downwards by 23%, the corrected value of the geometric mean would have been 9.6 /¿g g" 1 , representing an increase by a factor of 3.3 instead of the factor of 2.6 shown in Table 1. It is unlikely that this bias would have obscured a significant increase in lead concentrations, except perhaps in the roseate terns at Cedar Beach. Differential Temporal Exposure
Feathers are useful indicators of exposure to metals in birds because they reflect the levels of the metals circulating in the blood at the time when the feather was growing (Braune and Gaskin, 1987a, 1987b). However, circulating levels of metals in the blood are derived not only from current exposure, but also by mobilization from various organs in which the metals are stored (Osborn, 1979). Once feather growth is completed, the blood supply atrophies, the feathers become physiologically isolated from other tissues, and their metal content is extremely resistant to further change under the influence of heat, light or other forms of weathering, with very little evidence for contamination under field conditions (Applequist et al., 1984; Goede and de Bruin, 1984; Walsh, 1990). Further, the pooling of a number of small body feathers can minimize variations
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in the concentrations of metals in feathers dependent on the stage of molt (Furness et al., 1986). In our study, there were no significant changes in lead and cadmium concentrations in the regrown versus the initial feathers, but there were significant increases in mercury levels in both species of tern, and in selenium levels in roseate terns. These data clearly indicate that exposure to mercury on the breeding grounds was much higher than that on the wintering grounds. Mercury levels in common terns increased by a factor of about 3 at Cedar Beach, and by a factor of about 21 at Bird Island. Mercury levels in feathers of roseate terns at Cedar Beach increased by a factor of about 3, similar to that in common terns at the same site. Any bias resulting from the use of incompletely grown feathers would have led to underestimation of these differences, as discussed above. Several studies have shown that feathers are a major excretory pathway for mercury in seabirds, including gulls and terns (Braune, 1987; Braune and Gaskin, 1987a, 1987b; Furness et al., 1986, 1990). In Bonaparte's gulls (Larus Philadelphia), the total content of Hg in the body (excluding the feathers) declined by 88% during the period of autumn molt. Redistribution of mercury into the growing feathers accounted for about 64% of gross losses, and 106% of net losses, from the body during this period (Braune and Gaskin, 1987b). After the molt, feathers included about 93% of the total load of mercury carried by the birds (Braune and Gaskin, 1987a). In red-billed gulls (L novaehollandiae), mercury concentrations in feathers did not increase with age (Furness et al., 1990), indicating that most or all of the mercury accumulated in the body is eliminated with each molt. Although data on terns are limited (Braune, 1987), terns are closely related to gulls and would be expected to be similar in these toxicokinetic characteristics. Hence it would be expected that mercury concentrations in the initial feather collections would reflect the birds' exposure prior to the spring molt (i.e., in the winter quarters between October and April), whereas mercury concentrations in the regrown feathers would reflect the birds' exposure between the spring molt and the time of collection in June. Only part of this exposure would have taken place on the breeding grounds, and it is unlikely that the birds' body burdens would have reached steady state within the 30-50 days after arrival there. Hence, the 3- to 21-fold increases in mercury concentrations observed between the initial and regrown feather collections would not fully reflect the differences in exposure. No data appear to have been published on the importance of feathers as a route of excretion of lead, cadmium, or selenium in seabirds. It is possible that some of the body burdens may be retained through each molt. Hence, it is not clear that the differences between concentrations of these metals in the initial and regrown feathers would accurately reflect differences in exposure. Although the significant increase in sele-
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nium levels in roseate terns (Table 1) presumably indicates an increase in exposure, the magnitude of this increase may be understated, and other significant changes could have been missed. Overall, our data indicate that both species are much more highly exposed to mercury, roseate terns are more highly exposed to selenium, and both species may be more highly exposed to cadmium on their breeding grounds than in their winter quarters. These results probably reflect the fact that both breeding locations are in the industrial northeastern United States, where concentrations of these metals in marine sediments are elevated (O'Conner and Ehler, 1991). Differences Between Locations In the initial collections of common tern feathers, concentrations of lead, mercury, and cadmium were significantly higher at Cedar Beach than at Bird Island (Table 2). The main winter quarters of common terns are in eastern South America, from Trinidad to southern Brazil (Austin, 1953). Banding data suggest that common terns from colonies in New York and Massachusetts, including Cedar Beach and Bird Island, overlap widely or completely in autumn migration and in winter quarters (Austin, 1953; unpublished data of the authors). Hence, we would not have predicted differences in the initial concentrations. In the case of lead, there was a similar difference in concentrations in the regrown feathers (Table 2), so the differences in the initial collection could have resulted from carryover of residues accumulated during the previous summer. This explanation, however, cannot account for the intercolony differences in levels of mercury and selenium. These differences suggest that common terns from these colonies may be differentially exposed to mercury and selenium in the winter quarters. This suggests that the birds from these colonies may be segregated in the winter quarters, either geographically or ecologically, possibilities that require investigation. In the regrown feathers, concentrations of lead were significantly higher at Cedar Beach. Some of the levels of these metals in both species of terns were notably high in relation to other data on inshore seabirds. Although both breeding sites are located in polluted regions (O'Conner and Ehler, 1991), there is little information to associate the exposures with specific local sources. At Cedar Beach, both species of tern feed mainly within 10 km of the colony (Safina, 1990), an area characterized by suburban and recreational development with no known major sources of metal pollution except for heavy automobile traffic and industrialized areas (New York City, northern New jersey) 100-200 km to the west and southwest. At Bird Island, common terns feed mainly within 20 km of the colony in Buzzards Bay (including a few birds in New Bedford Harbor) and Vineyard Sound (Nisbet, 1981, 1983, and unpublished observations; D. Heinemann, personal communication). New Bedford Harbor is highly polluted with lead and cadmium, among other pollutants (Genest and
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Hatch, 1981; Sears and Battaglia, 1990, Summerhayes et al., 1977), which may explain the high concentrations of cadmium in a few of the birds from Bird Island (Table 1). However, there is little evidence that New Bedford is a major source of mercury, and the highest concentration of mercury found in sediment in a recent survey of Buzzards Bay was only 0.4 /tg g" 1 (Sears and Battaglia, 1990). This would not account for the strikingly and uniformly high levels of mercury in the regrown feathers of common terns at Bird Island (Table 1). Further investigation of the sources of mercury in the terns at Bird Island is needed.
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Differences Between Species
The species difference at Cedar Beach is interesting because both species feed in the same general area on the same species of fish during the breeding season (Safina, 1990), although roseates take smaller individuals. Roseate terns had significantly lower lead and selenium levels in their breast feathers when they arrived on the breeding grounds than common terns. However, levels in regrown feathers for the birds feeding near Cedar Beach were not significantly different with respect to species (except for selenium). This suggests that roseate and common terns at Cedar Beach are exposed to similar levels of these metals in their food, and that species differences primarily reflect exposure on the wintering ground. Overall, the levels and patterns of occurrence of metals in initial and regrown feathers suggest that initial species and locational differences may be due to differences in exposure on the wintering grounds, and that their exposure on the breeding grounds may be equal to (or much greater than, in the case of mercury) their exposure on the wintering grounds. REFERENCES Applequist, H., Asbirk, S., and Draback, L. 1984. Mercury monitoring: Mercury stability in bird feathers. Mar. Pollut. Bull. 15:22-27. Austin, O. L., Sr. 1953. The migration of the common tern (Sterna hirundo) in the Western Hemisphere. Bird-Banding 24:39-55. Braune, B. M. 1987. Comparison of total mercury levels in relation to diet and molt for nine species of marine birds. Arch. Environ. Toxicol. Contam. 16:217-224. Braune, B. M., and Gaskin, D. E. 1987a. Mercury levels in Bonaparte's gull (Larus Philadelphia) during autumn molt in the Quoddy region, New Brunswick, Canada. Arch. Environ. Contam. Toxicol. 16:539-549. Braune, B. M., and Gaskin, D. E. 1987b. A mercury budget for the Bonaparte's gull during autumn moult. Ornis Scand. 18:244-250. Burger, J. 1989. Least tern populations in coastal New Jersey: Monitoring and managing of a regionally endangered species. J. Coastal Research 5:801-811. Burger, J. 1992. Ecological effects of exposure to hazardous waste sites. In Evaluation and Management of Hazardous Waste, eds. J. A. Moore, B. V. Subramanyam and R. G. Tardiff. London: Wiley, in press.
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Risebrough, R. W., Sibley, F. C., and Kirven, M. N. 1971. Reproductive failure of the brown pelican on Anacapa Island in 1969. Am. Birds 25:8-9. Safina, C. 1990. Foraging habitat partitioning in roseate and common terns. Auk 107:351-358. SAS Institute, Inc. 1985. SAS User's Guide, 1985 Edition. Cary, N.C.: SAS Institute, Inc. Sears, J. R., and Battaglia, J. 1990. Use of benthic seaweeds to monitor heavy metals in Buzzards Bay, adjacent estuaries and New Bedford Harbor, Massachusetts. Technical Report 87-10 to Massachusetts Department of Environmental Protection. Southern Massachusetts University, North Dartmouth, Mass. Summerhayes, C. P., Ellis, J. P., Stoffers, P., Briggs, S. R., and Fitzgerald, M. G. 1977. Fine-grained sediment and industrial waste distribution and dispersal in New Bedford Harbor and western Buzzards Bay, Massachusetts. Woods Hole Oceanographic Institute Tech. Rep. WHOI-76-115, Woods Hole, Mass. Walsh, P. M. 1990. The use of seabirds as monitors of heavy metals in the marine environment. In Heavy Metals in the Marine Environment, eds. R. W. Furness and P. S. Rainbow, pp. 183-204. Boca Raton, Fla.: CRC Press. Received February 17, 1992 Accepted June 9, 1992
