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Temporal Trends in Metal Levels in Eggs of the Endangered Roseate Tern (Sterna dougallii) in New York
ENVIRONMENTAL RESEARCH, SECTION A ARTICLE NO.
77, 36—42 (1998)
ER973802
Temporal Trends in Metal Levels in Eggs of the Endangered Roseate Tern (Sterna dougallii ) in New York Michael Gochfeld*,-, 1 and Joanna Burger- ,‡ *Environmental and Community Medicine, UMDNJ-Robert Wood Johnson Medical School, Piscataway, New Jersey 08854-5635; -Environmental and Occupational Health Sciences Institute, Piscataway, New Jersey 08855-1179; and ‡Graduate Program in Ecology and Evolution, Biological Sciences, Rutgers University, Piscataway, New Jersey 08855-1059 Received August 5, 1996
impact on the population requires study. Female birds sequester certain organic and inorganic compounds in their eggs which have been widely used as a bioindicator for examining the body burdens of contaminants and therefore the temporal and spatial trends of the contaminants in the environment. The same analyses can also reflect the status or vulnerability of the indicator species. Extensive bridge deleading activities in the New York Bight (Cape May to Montauk) in the early 1990s coincided with a long-term study of the endangered roseate tern (Sterna dougallii ) on Long Island, New York, affording the opportunity to test the utility of such fish-eating species as bioindicators of lead contamination, as well as the potential impact on the bird population itself. In this paper we test the null hypothesis that there were no temporal trends between 1989 and 1994 in metal levels in eggs of roseate terns nesting at Cedar Beach, Long Island, where the birds have been declining since the late 1980s. We report levels and trends for cadmium, chromium, manganese, mercury, and selenium as well as lead in abandoned eggs collected each year. There were significant interyear differences for all metals, with 1990 to 1992 generally having higher levels than 1989 and 1994. The yearly differences were particularly prominent for lead, where the 10-fold increase may have been partially due to the increased removal of leaded paint from bridges in the early 1990s, leading to increased lead in the aquatic environment. Cadmium and chromium are also released during de-leading. The causes for the higher levels in the other metals in the early 1990s are unclear. Metal levels in roseate tern eggs are several times higher than the median reported for most birds, and the possible
Key Words: Sterna dougallii ; terns; lead; cadmium; mercury; chromium; manganese; selenium; bioindicator. INTRODUCTION
Environmental contaminants can bioaccumulate over time to reach toxic or even lethal levels unless organisms have the capacity to detoxify or excrete them. Many contaminants, particularly metal compounds, are persistent in nature and can accumulate in tissues such that levels increase with the age of the organism and with each succeeding step in the food chain. Concentrations in long-lived and toplevel carnivores can reach levels that are much higher than at lower trophic levels or than levels measured in environmental media such as soil and water (van Straalen and Ernst, 1991; Burger et al., 1992; Sundlof et al., 1994). Seabirds are particularly vulnerable because they are long-lived, are often high on the food chain, and live in coastal environments near urban, industrial, or agricultural sources, where human-generated contaminant levels may be high (Burger, 1993). Moreover, some seabird species have concentrations of contaminants such as cadmium, mercury, and selenium that are in the range that would cause toxic effects in terrestrial bird species (see review in Nisbet, 1993). Birds can excrete contaminants directly and can sequester them in their feathers (Braune, 1987; Lewis and Furness, 1991), and females can excrete them in their eggs and eggshells (Fimreite et al., 1982; Burger and Gochfeld, 1991a, b, 1993; Burger, 1994). In addition, Kim et al. (1996) recently suggested that some pelagic seabirds (albatrosses and petrels) can demethylate methyl mercury in the liver,
1 To whom correspondence should be addressed at EOHSI, 681 Frelinghuysen Rd., Piscataway, NJ 08855-1179. Fax: (732) 4450130. E-mail: [email protected]. 36 0013-9351/98 $25.00 Copyright ( 1998 by Academic Press All rights of reproduction in any form reserved.
( 1998
Academic Press
TEMPORAL TRENDS IN METALS IN ROSEATE TERN EGGS
and then store inorganic mercury. For most birds, feathers and eggs can serve as bioindicators of internal contamination (Goede and deBruin, 1984, 1986; Furness et al., 1986; Burger, 1993) without the need for sacrificing otherwise healthy adults. These levels can then be used to assess whether there are potential reproductive problems in these populations (Burger, 1994). In this paper we examine the levels of cadmium, chromium, lead, manganese, mercury, and selenium in the eggs of roseate terns (Sterna dougallii) breeding in a colony on Long Island, New York, from 1989 through 1994. This was a period of their severe decline on western Long Island. We test the null hypothesis that there were no differences or temporal trends in metal concentrations from 1989 through 1994. Roseate terns breed in eastern North America, Europe, North Africa, Asia, and the Australasian region, but are not abundant anywhere (Gochfeld, 1983). Many of the populations in North America and Europe that have been well documented have been declining over the past two decades. The Northeastern United States population declined dramatically from the 1950s to the 1970s (Nisbet, 1980), leading to its placement on the U.S. federal endangered species list. In Northeastern North America, 90% of the regional metapopulation breeds in the area from Cape Cod, Massachusetts, to the south shore of Long Island, New York (Gochfeld et al., 1997), and in the late 1980s and early 1990s, most bred at only four colony sites (Spendelow et al., 1995). To understand possible options for management and recovery, a cooperative study of the metapopulation dynamics of this species was undertaken at these four colonies (Spendelow et al., 1995), but few data are available on the possible role of toxic chemicals in population declines of this or any species. This study examined egg levels in roseate terns nesting at Cedar Beach, New York, the southernmost major colony. MATERIALS AND METHODS
Under appropriate state and federal collecting permits, eggs of roseate terns were salvaged from abandoned nests at Cedar Beach, western Suffolk County, Long Island, New York, each year between 1989 and 1994. The colony at Cedar Beach is located in an interdune area vegetated mainly with Beach Grass (Ammophila breviligulata), grasses and Seaside Goldenrod (Solidago sempervirens; (Gochfeld, 1976; Burger et al., 1996). During the sampling period between 60 and 100 pairs of roseate terns nested
37
each year, in a colony that also contained 100—300 pairs of black skimmers (Rynchops niger) and up to 3000 pairs of common terns (Sterna hirundo, Burger and Gochfeld, 1991a). Sample sizes varied depending on the number of abandoned nests caused by a variety of factors: inclement weather (early nests frequently abandoned during periods of prolonged cold rain), predators (high numbers of predators sometimes caused early pairs to abandon first eggs), aggressive neighbors, human disturbance and trapping, and late nesting (some late nesting pairs abandoned their nests). In some cases a first chick hatched and was led to a more protective shelter, leaving behind the unhatched second egg. Some eggs failed to hatch due to infertility or embryonic mortality and were abandoned. The possible role of chemicals influencing adult behavior as a cause of abandonment is unknown, but since there were many different causes of abandonment throughout the season, particularly early (May) and late (July), it is unlikely that toxic effects contributed significantly to abandonment as a whole. In 1995 the entire colony abandoned due to predation, and there was no nesting in 1996, so no eggs are available for those years. Eggs were refrigerated until digested for later analysis. All eggs each year were analyzed in a batch and the interval between collection and analysis was 1—4 weeks. Archived specimens from earlier years were analyzed as a batch in 1996. All specimens were analyzed in the Elemental Analysis Laboratory of the Environmental and Occupational Health Sciences Institute in Piscataway, New Jersey. Egg contents were homogenized and digested individually in warm nitric acid mixed with the addition of 30% hydrogen peroxide, and subsequently diluted with deionized water. Mercury was analyzed by cold vapor technique, and the other elements were analyzed by graphite furnace atomic absorption (Burger and Gochfeld, 1991b). All concentrations are expressed in nanograms per gram (ppb) on a wet weight basis. Detection limits were 0.02 ppb for cadmium, 0.08 ppb for chromium, 0.15 ppb for lead, 0.09 ppb for manganese, 50 ppb for mercury, and 0.7 ppb for selenium. At these detection limits only 4 of 70 eggs could not be quantified for lead, 3 for cadmium, and 6 (all in 1994) for chromium. All specimens were analyzed in batches with blanks, a standard calibration curve, and spiked specimens. Batches with recoveries on spiked samples of less than 85% or more than 115% were reanalyzed. The coefficient of variation on replicate, spiked samples ranged up to 10%.
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All metal data were log-transformed, allowing parametric analysis, and analysis of variance with Duncan multiple range tests were performed to distinguish significant differences. Both arithmetic and geometric means are given to facilitate comparisons with other studies.
tions included lead and selenium (r"0.33, P\ 0.0002), lead and chromium (r"0.37, P\0.0001), cadmium and manganese (r"0.18, P\0.04), and selenium and chromium (r"0.41, P\0.0001). The only significant negative correlation was between cadmium and mercury (r"!0.27, P\0.002).
RESULTS
DISCUSSION
Yearly Differences
Metal concentration results are shown in Table 1 and Fig. 1.
We predicted that there would be significant differences among years for some metals based on anthropogenic inputs (particularly bridge de-leading) as well as variations in feeding areas. Two different yearly patterns in metal levels in the eggs of roseate terns were evident: (1) relatively low levels in 1989 and 1994 with higher levels in between (lead, cadmium, manganese, chromium, and selenium), and (2) generally decreasing levels with time (mercury, except for 1993). No metal had its highest value in 1994, probably reflecting a true decline in exposure, and three metals (cadmium, manganese, and selenium) were highest in 1992. This partly may reflect changes in preferred feeding areas corresponding to prey abundance, as well as temporal variation in contaminants. Lead is a major pollutant in the New York Bight ecosystem (O’Connor and Stanford, 1979; Mueller et al., 1976; Squibb et al., 1991), so it is not surprising that levels are present in the eggs of birds that acquire resources in the New York region prior to egg-laying. However, the lead levels are of interest
Yearly Differences in Metal Levels ANOVA shows significant models (P\0.01) for all metals except manganese (P"0.06), although the differences were particularly prominent for lead, chromium, and selenium (Table 2). In this model, year contributed between 17% (manganese) and 54% (chromium) to the variance. In general, metal levels were higher in 1992 than in other years for cadmium, manganese, and selenium. No metal showed a signifiant temporal trend across all years, although lead decreased from 1990 to 1994, mercury decreased from 1989 to 1994 (except 1993), and chromium increased from 1989 to 1993. Correlations among Metals There were few significant correlations when the whole data set is taken together. Positive correla-
TABLE 1 Concentrations of Metals (ppb, Wet Weight, Mean 6 Standard Error) in the Eggs of Roseate Terns from Cedar Beach, Long Island Metal Number of eggs Number of pairsa Cadmium Chromium Lead Manganese Mercury Selenium
1989
1990
1991
1992
1993
1994
12 66 21$7 (2.5) 82$12 (76) 235$78 (92) 3350$293 (3280) 1580$222 (1490) 1330$159 (1290)
10 94 51$30 (21) 285$28 (274) 2670$425 (2440) 3250$170 (3210) 1390$88 (1360) 2530$1250 (2490)
5 81 91$50 (55) 153$37 (142) 2180$368 (2050) 3150$129 (3140) 1050$134 (1020) 1480$134 (1460)
13 80 189$49 (120) 2520$462 (2118) 2290$673 (1493) 4110$270 (4000) 1070$94 (1020) 3960$522 (3660)
10 58 40$17 (19) 3070$764 (1678) 505$166 (385) 3400$251 (3330) 1420$122 (1370) 1980$237 (1750)
20 70 74$12 (64) 45$11 (8) 272$78 (85) 3550$155 (3500) 1100$52 (1070) 1680$61 (1660)
Note. Given also are geometric means (in parenthesis). All values rounded to three significant figures. a 100 breeding pairs in 1987, and 93 pairs in 1988. 40 pairs began to nest in 1995 but deserted the colony due to predators, and none nested in 1996.
TEMPORAL TRENDS IN METALS IN ROSEATE TERN EGGS
39
FIG. 1. Arithmetic mean on untransformed data (horizontal bar), standard error (box), and range (vertical line) for metal levels (ppb, wet weight) in eggs of roseate terns from 1989 to 1994. All data in ppb (ng/g) wet weight. For sample sizes see Table 1. Letters at top or bottom of each panel indicate statistical significance (P\0.05) among years. Years sharing the same letter are not different.
because there was nearly a 10-fold increase in lead in the years 1990—1992 compared to the other years. The pattern for lead is probably largely explained by the increase in the removal of paint from the many bridges in the New York estuary region in the early 1990s, associated with significant elevations of lead levels in bridge workers (NJDOH, 1988). Lead levels declined when remediation was completed. We did not find corresponding sediment or fish data. Cadmium and chromium are also released during the de-leading operations (Conroy et al., 1995). Lead paint removal from bridges is a known source of lead, chromium, and cadmium exposure for both
workers and the environment (NJDOH, 1988; CDC, 1989; Conroy et al., 1995). Relative Levels of Metals It is useful to compare the level of metals in the eggs of the roseate terns with those from other species (Table 3). We reviewed reports of metals in bird eggs, finding two papers referring to selenium and manganese and up to 44 papers on mercury in bird eggs. The papers were published over a period of two decades and reflect not only great taxonomic and ecologic diversity of the birds represented but also
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GOCHFELD AND BURGER
TABLE 2 Significant ANOVA Models for the Effect of Year on the Variance (df 5 5, 64)
Cadmium Chromium Lead Manganese Mercury Selenium
r2
F value
P
0.28 0.54 0.44 0.17 0.26 0.52
4.8 13.3 10.1 2.3 4.1 11.0
0.0009 0.0001 0.0001 0.06 0.003 0.0001
Note. Log-transformed data used.
geographic and methodologic diversity. Given this variability in existing data, we found that levels of cadmium, chromium, lead, and mercury in this study were all above the median of levels reported in other studies. The average level of chromium in the eggs of roseate terns was over 15 times higher than the median reported in the literature; cadmium and lead were 8 times higher, and mercury was over 3 times higher (Table 3). Thus, metal levels in roseate tern eggs on Long Island were relatively high, and the possibility of adverse reproductive effects requires scrutiny. To date there is no evidence of significant rates of infertility, embryonic mortality, or developmental defects for roseate terns (Gochfeld et al., 1997). Few studies report levels of selenium in bird eggs. King et al. (1983) and Ohlendorf and Harrison (1986) report levels from uncontaminated sites (Table 3) which are lower than we found for roseate eggs. Selenium levels from Franklin’s gull eggs in
TABLE 3 Levels of Metals in Eggs of Birds (ppb Adapted from Review by Burger, 1994)
Metal Cadmium Chromium Lead Manganesea Mercury Seleniumb
Number of studies or locations 26 10 25 2 44 2
Range of mean levels (ppb) 2—530 10—370 20—6700 500—4000 70—7290 300—2100
Mean level for all roseate eggs Median (1989—1994) 10 70 140 2250 33 1200
80 1100 1150 3540 1230 2310
Note. Given are ranges and median of the mean values (converted to ppb) as reported in a number of studies for each metal which vary geographically, taxonomically, and methodologically. a From Burger and Gochfeld, 1995, 1996. b From Ohlehdorf and Harrison, 1986; King et al., 1983.
Minnesota, however, averaged nearly 3 ppm (Burger and Gochfeld, 1996), which are higher than those reported here. Eggs from contaminated sites such as Kesterson in California, however, can have levels as high as 81 ppm which are grossly embryotoxic (Hoffman et al., 1988). Ohlendorf (1993) lists the toxic level as higher than 8 ppm. Thus, although the levels of selenium in roseate terns are at the high end for birds, they are not in the toxic range. Even fewer studies report manganese levels in eggs. We found mean levels of from 3 to 4 ppm for herring gulls in the same nesting area as the roseates in this study (Burger and Gochfeld, 1995). Long-Term Effects Roseate terns are a federally endangered species in the United States and Canada, and their populations have declined or remained stable while other closely related terns have not suffered. Although the causes of reproductive losses at any given colony are usually inclement weather, food shortage, or predators (Nisbet, 1980; Burger et al., 1995; Gochfeld et al., 1997), toxics may be a contributory factor. Toxics could interfere with fertility, reproductive behavior, embryonic development, chick maturation, or survival. This research was partly undertaken to determine if there were high levels of any metals in the eggs that might suggest possible developmental defects or lowered reproductive success, if there were increases in any metals over the period of decline, and if there were sufficiently high levels of any metals, compared to other local-nesting seabirds, to suggest that roseate terns may be more highly exposed and thus vulnerable. Nisbet (1993) found little direct evidence that the reproductive rate of seabirds has been impaired by heavy metals. Gochfeld (1980) attributed developmental defects in common terns of New York to elevated mercury levels. Hoffman et al. (1988) documented embryotoxicity of selenium in waterbirds in California. Mercury is particularly of interest because the lowest observed effect level (LOEL) from a variety of laboratory studies is about 1 ppm in eggs (Eisler, 1987; Burger, 1993). The mean levels of mercury in eggs of roseate terns were 1 ppm or higher for all six years, and it is during this period that the roseate terns decreased sharply in numbers. Although the proximate cause of lowered reproductive success was often predation, predation rates can be increased by a decrease in parental attentiveness and a decrease in chick nest site fidelity that can be affected by mercury. Although the harvesting of adult terns on the wintering grounds is likely to be the major factor
TEMPORAL TRENDS IN METALS IN ROSEATE TERN EGGS
affecting roseate tern populations (Gochfeld et al., 1997), the effects of pollutants may reduce hatching or chick survival, thereby preventing the population from compensating for the harvest. A 6-year period of annual sampling is not sufficient to detect long-term trends or cyclical fluctuations. Bioindicators such as the roseate tern eggs are valuable both for testing hypotheses about spatial and temporal trends or about remediation and for generating hypotheses as well. Although we have a convincing explanation for the increase followed by a decrease in the lead, chromium, and cadimium levels (1990—1992 vs 1993—1994), there is no comparable explanation for manganese and selenium. ACKNOWLEDGMENTS We thank I. C. T. Nisbet, H. Ohlendorf, and R. Furness for valuable discussions about toxicants; Robert Paxton and Sarah Plimpton and Carl Safina and Mercedes Lee for advice, logistical help, and accommodations over the years; and T. Shukla, J. Ondrof, R. Ramos, and T. Benson for laboratory analyses in the laboratory. Support for the analyses was provided by the U.S. Fish and Wildlife Service under a cooperative agreement; by NIEHS Grant ESO 5022; by the Consortium for Risk Evaluation with Stakeholder Participation (CRESP, Department of Energy AI No. DE-FC01-95EW55084); and by the Environmental and Occupational Health Sciences Institute. We thank the U.S. Fish and Wildlife Service and the New York State Department of Environmental Conservation for permits to collect specimens and conduct this research. Our procedures were approved by the Rutgers University Animal Review Board.
REFERENCES Braune, B. W. (1987). Comparison of total mercury levels in relation to diet and molt for nine species of marine birds. Archiv. Environ. Contam. Toxicol. 16, 217—224. Burger, J. (1993). Metals in avian feathers: Bioindicators of environmental pollution. Rev. Environ. Toxicol. 5, 203—311. Burger, J. (1994). Heavy metals in avian eggshells: Another excretion method. J. Toxicol. Environ. Health 41, 207—220. Burger, J., and Gochfeld, M. (1991a). ‘‘The Common Tern: Its Breeding Biology and Social Behavior.’’ Columbia Univ. Press, Columbia, NY. Burger, J., and Gochfeld, M. (1991b). Cadmium and lead in common terns (Aves: Sterna hirundo): Relationship between levels in parents and eggs. Environ. Monit. Assess. 16, 253—258. Burger, J., and Gochfeld, M. (1993). Lead and cadmium accumulation in eggs and fledgling seabirds in the New York Bight. Environ. Toxicol. Chem. 12, 261—267. Burger, J., and Gochfeld, M. (1995). Heavy metal and selenium concentrations in eggs of herring gulls (Larus argentatus): Temporal differences from 1989 to 1994. Arch. Environ. Contam. Toxicol. 29, 192—197. Burger, J., and Gochfeld, M. (1996). Heavy metal and selenium levels in Franklin’s gull (Larus pipixcan): Parents and their eggs. Arch. Environ. Contam. Toxicol. 30, 487—491.
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Burger, J., Cooper, K., Saliva, J., Gochfeld, D., Lipsky, D., and Gochfeld, M. (1992). Mercury bioaccumulation in organisms from three Puerto Rican estuaries. Environ. Monit. Assess. 22, 181—197. Burger, J., Nisbet, I. C. T., Safina, C., and Gochfeld, M. (1996). Temporal patterns in reproductive success in the endangered roseate tern (Sterna dougallii) nesting on Long Island, New York, and Bird Island, Massachusetts. Auk 113, 131—142. Center for Disease Control (CDC). (1989). Poisoning in bridge demolition workers—Massachusetts. Morbid. Mortal. Week. Rev. 38, 692—694. Conroy, L. M., Lindsay, R. M. M., and Sullivan, P. M. (1995). Lead, chromium, and cadmium emission factors during abrasive blasting operations by bridge painters. Amer. Ind. Hyg. Assoc. J. 56, 266—271. Eisler, R. (1987). Mercury hazards to fish, wildlife, and invertebrates: A synoptic review. U.S. Fish Wildlife Ser. Biol. Rep. 85, (1.1). Fimreite, N., Brevik, F., and Trop, R. (1982). Murcury and organochlorines in eggs from a Norwegian gannet colony. Arch. Environ. Contam. Toxicol. 28, 58—60. Furness, R. W., Muirhead, S. J., and Woodburn, M. (1986). Using bird feathers to measure mercury in the environment: Relationship between mercury content and moult. Mar. Pollut. Bull. 17, 27—37. Gochfeld, M. (1976). Waterbird colonies of Long Island, New York. 3. The Cedar Beach ternery. Kingbird 26, 62—80. Gochfeld, M. (1983). The roseate tern: World distribution and status of a threatened species. Biol. Conserv. 25, 103—125. Gochfeld, M., Burger, J., and Nisbet, I. C. T. (1998). ‘‘Roseate tern. Birds of North America.’’ American Ornithologists’ Union, Philadelphia, PA. [in press] Goede, A. A., and deBruin, M. (1984). The use of bird feather parts as a monitor for metal pollution. Environ. Pollut. 8, 281—289. Goede, A. A., and deBruin, M. (1986). The use of feathers for indicating heavy metal pollution. Environ. Monit. Assess. 7, 249—256. Hoffman, D. J., Ohlendorf, H. M., and Aldrich, T. W. (1988). Selenium teratogenesis in natural populations of aquatic birds in central California. Arch. Environ. Contam. Toxicol. 17, 519—525. Kim, E. Y., Murakami, T., Saeki, K., and Tatsukawa, R. (1996). Mercury levels and its chemical form in tissues and organs of seabirds. Arch. Environ. Contam. Toxicol. 30, 259—266. King, K. A., Lefever, C. A., and Mulhern, B. M. (1988). Organochlorine and metal levels in royal terns nesting on the central Texas coast. J. Field Ornithol. 54, 295—303. Lewis, S. A., and Furness, R. W. (1991). Mercury accumulation and excretion by laboratory reared black-headed gulls (Larus ridibundus) chicks. Arch. Environ. Contam. Toxicol. 21, 316—320. Mueller, J. A., Heris, J. S., Anderson, A. R., and Hughes, C. F. (1976). ‘‘Contaminant Inputs to the New York Bight: Priorities for Research.’’ NOAA Technical Memorandum ERL MESA-6, Natl. Oceanic Atmospheric Admin., Washington, DC. New Jersey Department of Health (NJDOH). (1988). ‘‘A Report on Lead Exposure at the Rts 1 and 9 Bridge Construction Site, Newark, N.J.’’ Health hazards evaluation program, Trenton, NJ.
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Nisbet, I. C. T. (1980). ‘‘Status and Trends of the Roseate Tern Sterna dougallii in North America and the Caribbean.’’ U.S. Fish and Wildlife Service, Newton Corner, MA. [Unpubl. report] Nisbet, I. C. T. (1993). Effects of pollution on marine birds. In ‘‘Seabirds on Islands: Threats, Case Studies, and Action Plans,’’ (D. N. Nettleship, J. Burger, and M. Gochfeld, Eds.), pp. 8—25. International Council on Bird Preservation, Cambridge, England. O’Connor, J. S., and Stanford, H. M. (1979). ‘‘Chemical Pollutants of the New York Bight: Priorities for Research,’’ NOAA Special Report, Natl. Oceanic Atmospheric Admin., Washington, DC. Ohlendorf, H. M. (1993). Marine birds and trace elements in the temperate North Pacific. In ‘‘The Status, Ecology, and Conservation of Marine Birds of the North Pacific,’’ (K. Vermeer, K. T.
Briggs, K. H. Morgan, and D. Siegel-Causey, Eds). Can. Wildl. Serv. Spec. Publ. Ottawa, Canada. Ohlendorf, H. M., and Harrison, C. S. (1986). Mercury, selenium, cadmium and organochlorines in eggs of three Hawaiian seabird species. Environ. Pollut. 11B, 169—191. Spendelow, J. A., Nichols, J. D., Nisbet, I. C. T., Hays, H., Cormons, G. D., Burger, J., Safina, C., Hines, J. E., and Gochfeld, M. (1995). Estimating annual survival and movement rates of adults within a metapopulation of Roseate terns. Ecology 76, 2415—2428. Sundlof, S. F., Spalding, M. G., Wentworth, J. D., and Steible, C. K. (1994). Mercury in livers of wading birds (Ciconiiformes) in southern Florida. Arch. Environ. Contam. Toxicol. 27, 299—305. van Straalen, N. M., and Ernst, E. (1991). Metal biomagnification may endanger species in critical pathways. Oikos 62, 255—256.
77, 36—42 (1998)
ER973802
Temporal Trends in Metal Levels in Eggs of the Endangered Roseate Tern (Sterna dougallii ) in New York Michael Gochfeld*,-, 1 and Joanna Burger- ,‡ *Environmental and Community Medicine, UMDNJ-Robert Wood Johnson Medical School, Piscataway, New Jersey 08854-5635; -Environmental and Occupational Health Sciences Institute, Piscataway, New Jersey 08855-1179; and ‡Graduate Program in Ecology and Evolution, Biological Sciences, Rutgers University, Piscataway, New Jersey 08855-1059 Received August 5, 1996
impact on the population requires study. Female birds sequester certain organic and inorganic compounds in their eggs which have been widely used as a bioindicator for examining the body burdens of contaminants and therefore the temporal and spatial trends of the contaminants in the environment. The same analyses can also reflect the status or vulnerability of the indicator species. Extensive bridge deleading activities in the New York Bight (Cape May to Montauk) in the early 1990s coincided with a long-term study of the endangered roseate tern (Sterna dougallii ) on Long Island, New York, affording the opportunity to test the utility of such fish-eating species as bioindicators of lead contamination, as well as the potential impact on the bird population itself. In this paper we test the null hypothesis that there were no temporal trends between 1989 and 1994 in metal levels in eggs of roseate terns nesting at Cedar Beach, Long Island, where the birds have been declining since the late 1980s. We report levels and trends for cadmium, chromium, manganese, mercury, and selenium as well as lead in abandoned eggs collected each year. There were significant interyear differences for all metals, with 1990 to 1992 generally having higher levels than 1989 and 1994. The yearly differences were particularly prominent for lead, where the 10-fold increase may have been partially due to the increased removal of leaded paint from bridges in the early 1990s, leading to increased lead in the aquatic environment. Cadmium and chromium are also released during de-leading. The causes for the higher levels in the other metals in the early 1990s are unclear. Metal levels in roseate tern eggs are several times higher than the median reported for most birds, and the possible
Key Words: Sterna dougallii ; terns; lead; cadmium; mercury; chromium; manganese; selenium; bioindicator. INTRODUCTION
Environmental contaminants can bioaccumulate over time to reach toxic or even lethal levels unless organisms have the capacity to detoxify or excrete them. Many contaminants, particularly metal compounds, are persistent in nature and can accumulate in tissues such that levels increase with the age of the organism and with each succeeding step in the food chain. Concentrations in long-lived and toplevel carnivores can reach levels that are much higher than at lower trophic levels or than levels measured in environmental media such as soil and water (van Straalen and Ernst, 1991; Burger et al., 1992; Sundlof et al., 1994). Seabirds are particularly vulnerable because they are long-lived, are often high on the food chain, and live in coastal environments near urban, industrial, or agricultural sources, where human-generated contaminant levels may be high (Burger, 1993). Moreover, some seabird species have concentrations of contaminants such as cadmium, mercury, and selenium that are in the range that would cause toxic effects in terrestrial bird species (see review in Nisbet, 1993). Birds can excrete contaminants directly and can sequester them in their feathers (Braune, 1987; Lewis and Furness, 1991), and females can excrete them in their eggs and eggshells (Fimreite et al., 1982; Burger and Gochfeld, 1991a, b, 1993; Burger, 1994). In addition, Kim et al. (1996) recently suggested that some pelagic seabirds (albatrosses and petrels) can demethylate methyl mercury in the liver,
1 To whom correspondence should be addressed at EOHSI, 681 Frelinghuysen Rd., Piscataway, NJ 08855-1179. Fax: (732) 4450130. E-mail: [email protected]. 36 0013-9351/98 $25.00 Copyright ( 1998 by Academic Press All rights of reproduction in any form reserved.
( 1998
Academic Press
TEMPORAL TRENDS IN METALS IN ROSEATE TERN EGGS
and then store inorganic mercury. For most birds, feathers and eggs can serve as bioindicators of internal contamination (Goede and deBruin, 1984, 1986; Furness et al., 1986; Burger, 1993) without the need for sacrificing otherwise healthy adults. These levels can then be used to assess whether there are potential reproductive problems in these populations (Burger, 1994). In this paper we examine the levels of cadmium, chromium, lead, manganese, mercury, and selenium in the eggs of roseate terns (Sterna dougallii) breeding in a colony on Long Island, New York, from 1989 through 1994. This was a period of their severe decline on western Long Island. We test the null hypothesis that there were no differences or temporal trends in metal concentrations from 1989 through 1994. Roseate terns breed in eastern North America, Europe, North Africa, Asia, and the Australasian region, but are not abundant anywhere (Gochfeld, 1983). Many of the populations in North America and Europe that have been well documented have been declining over the past two decades. The Northeastern United States population declined dramatically from the 1950s to the 1970s (Nisbet, 1980), leading to its placement on the U.S. federal endangered species list. In Northeastern North America, 90% of the regional metapopulation breeds in the area from Cape Cod, Massachusetts, to the south shore of Long Island, New York (Gochfeld et al., 1997), and in the late 1980s and early 1990s, most bred at only four colony sites (Spendelow et al., 1995). To understand possible options for management and recovery, a cooperative study of the metapopulation dynamics of this species was undertaken at these four colonies (Spendelow et al., 1995), but few data are available on the possible role of toxic chemicals in population declines of this or any species. This study examined egg levels in roseate terns nesting at Cedar Beach, New York, the southernmost major colony. MATERIALS AND METHODS
Under appropriate state and federal collecting permits, eggs of roseate terns were salvaged from abandoned nests at Cedar Beach, western Suffolk County, Long Island, New York, each year between 1989 and 1994. The colony at Cedar Beach is located in an interdune area vegetated mainly with Beach Grass (Ammophila breviligulata), grasses and Seaside Goldenrod (Solidago sempervirens; (Gochfeld, 1976; Burger et al., 1996). During the sampling period between 60 and 100 pairs of roseate terns nested
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each year, in a colony that also contained 100—300 pairs of black skimmers (Rynchops niger) and up to 3000 pairs of common terns (Sterna hirundo, Burger and Gochfeld, 1991a). Sample sizes varied depending on the number of abandoned nests caused by a variety of factors: inclement weather (early nests frequently abandoned during periods of prolonged cold rain), predators (high numbers of predators sometimes caused early pairs to abandon first eggs), aggressive neighbors, human disturbance and trapping, and late nesting (some late nesting pairs abandoned their nests). In some cases a first chick hatched and was led to a more protective shelter, leaving behind the unhatched second egg. Some eggs failed to hatch due to infertility or embryonic mortality and were abandoned. The possible role of chemicals influencing adult behavior as a cause of abandonment is unknown, but since there were many different causes of abandonment throughout the season, particularly early (May) and late (July), it is unlikely that toxic effects contributed significantly to abandonment as a whole. In 1995 the entire colony abandoned due to predation, and there was no nesting in 1996, so no eggs are available for those years. Eggs were refrigerated until digested for later analysis. All eggs each year were analyzed in a batch and the interval between collection and analysis was 1—4 weeks. Archived specimens from earlier years were analyzed as a batch in 1996. All specimens were analyzed in the Elemental Analysis Laboratory of the Environmental and Occupational Health Sciences Institute in Piscataway, New Jersey. Egg contents were homogenized and digested individually in warm nitric acid mixed with the addition of 30% hydrogen peroxide, and subsequently diluted with deionized water. Mercury was analyzed by cold vapor technique, and the other elements were analyzed by graphite furnace atomic absorption (Burger and Gochfeld, 1991b). All concentrations are expressed in nanograms per gram (ppb) on a wet weight basis. Detection limits were 0.02 ppb for cadmium, 0.08 ppb for chromium, 0.15 ppb for lead, 0.09 ppb for manganese, 50 ppb for mercury, and 0.7 ppb for selenium. At these detection limits only 4 of 70 eggs could not be quantified for lead, 3 for cadmium, and 6 (all in 1994) for chromium. All specimens were analyzed in batches with blanks, a standard calibration curve, and spiked specimens. Batches with recoveries on spiked samples of less than 85% or more than 115% were reanalyzed. The coefficient of variation on replicate, spiked samples ranged up to 10%.
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All metal data were log-transformed, allowing parametric analysis, and analysis of variance with Duncan multiple range tests were performed to distinguish significant differences. Both arithmetic and geometric means are given to facilitate comparisons with other studies.
tions included lead and selenium (r"0.33, P\ 0.0002), lead and chromium (r"0.37, P\0.0001), cadmium and manganese (r"0.18, P\0.04), and selenium and chromium (r"0.41, P\0.0001). The only significant negative correlation was between cadmium and mercury (r"!0.27, P\0.002).
RESULTS
DISCUSSION
Yearly Differences
Metal concentration results are shown in Table 1 and Fig. 1.
We predicted that there would be significant differences among years for some metals based on anthropogenic inputs (particularly bridge de-leading) as well as variations in feeding areas. Two different yearly patterns in metal levels in the eggs of roseate terns were evident: (1) relatively low levels in 1989 and 1994 with higher levels in between (lead, cadmium, manganese, chromium, and selenium), and (2) generally decreasing levels with time (mercury, except for 1993). No metal had its highest value in 1994, probably reflecting a true decline in exposure, and three metals (cadmium, manganese, and selenium) were highest in 1992. This partly may reflect changes in preferred feeding areas corresponding to prey abundance, as well as temporal variation in contaminants. Lead is a major pollutant in the New York Bight ecosystem (O’Connor and Stanford, 1979; Mueller et al., 1976; Squibb et al., 1991), so it is not surprising that levels are present in the eggs of birds that acquire resources in the New York region prior to egg-laying. However, the lead levels are of interest
Yearly Differences in Metal Levels ANOVA shows significant models (P\0.01) for all metals except manganese (P"0.06), although the differences were particularly prominent for lead, chromium, and selenium (Table 2). In this model, year contributed between 17% (manganese) and 54% (chromium) to the variance. In general, metal levels were higher in 1992 than in other years for cadmium, manganese, and selenium. No metal showed a signifiant temporal trend across all years, although lead decreased from 1990 to 1994, mercury decreased from 1989 to 1994 (except 1993), and chromium increased from 1989 to 1993. Correlations among Metals There were few significant correlations when the whole data set is taken together. Positive correla-
TABLE 1 Concentrations of Metals (ppb, Wet Weight, Mean 6 Standard Error) in the Eggs of Roseate Terns from Cedar Beach, Long Island Metal Number of eggs Number of pairsa Cadmium Chromium Lead Manganese Mercury Selenium
1989
1990
1991
1992
1993
1994
12 66 21$7 (2.5) 82$12 (76) 235$78 (92) 3350$293 (3280) 1580$222 (1490) 1330$159 (1290)
10 94 51$30 (21) 285$28 (274) 2670$425 (2440) 3250$170 (3210) 1390$88 (1360) 2530$1250 (2490)
5 81 91$50 (55) 153$37 (142) 2180$368 (2050) 3150$129 (3140) 1050$134 (1020) 1480$134 (1460)
13 80 189$49 (120) 2520$462 (2118) 2290$673 (1493) 4110$270 (4000) 1070$94 (1020) 3960$522 (3660)
10 58 40$17 (19) 3070$764 (1678) 505$166 (385) 3400$251 (3330) 1420$122 (1370) 1980$237 (1750)
20 70 74$12 (64) 45$11 (8) 272$78 (85) 3550$155 (3500) 1100$52 (1070) 1680$61 (1660)
Note. Given also are geometric means (in parenthesis). All values rounded to three significant figures. a 100 breeding pairs in 1987, and 93 pairs in 1988. 40 pairs began to nest in 1995 but deserted the colony due to predators, and none nested in 1996.
TEMPORAL TRENDS IN METALS IN ROSEATE TERN EGGS
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FIG. 1. Arithmetic mean on untransformed data (horizontal bar), standard error (box), and range (vertical line) for metal levels (ppb, wet weight) in eggs of roseate terns from 1989 to 1994. All data in ppb (ng/g) wet weight. For sample sizes see Table 1. Letters at top or bottom of each panel indicate statistical significance (P\0.05) among years. Years sharing the same letter are not different.
because there was nearly a 10-fold increase in lead in the years 1990—1992 compared to the other years. The pattern for lead is probably largely explained by the increase in the removal of paint from the many bridges in the New York estuary region in the early 1990s, associated with significant elevations of lead levels in bridge workers (NJDOH, 1988). Lead levels declined when remediation was completed. We did not find corresponding sediment or fish data. Cadmium and chromium are also released during the de-leading operations (Conroy et al., 1995). Lead paint removal from bridges is a known source of lead, chromium, and cadmium exposure for both
workers and the environment (NJDOH, 1988; CDC, 1989; Conroy et al., 1995). Relative Levels of Metals It is useful to compare the level of metals in the eggs of the roseate terns with those from other species (Table 3). We reviewed reports of metals in bird eggs, finding two papers referring to selenium and manganese and up to 44 papers on mercury in bird eggs. The papers were published over a period of two decades and reflect not only great taxonomic and ecologic diversity of the birds represented but also
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GOCHFELD AND BURGER
TABLE 2 Significant ANOVA Models for the Effect of Year on the Variance (df 5 5, 64)
Cadmium Chromium Lead Manganese Mercury Selenium
r2
F value
P
0.28 0.54 0.44 0.17 0.26 0.52
4.8 13.3 10.1 2.3 4.1 11.0
0.0009 0.0001 0.0001 0.06 0.003 0.0001
Note. Log-transformed data used.
geographic and methodologic diversity. Given this variability in existing data, we found that levels of cadmium, chromium, lead, and mercury in this study were all above the median of levels reported in other studies. The average level of chromium in the eggs of roseate terns was over 15 times higher than the median reported in the literature; cadmium and lead were 8 times higher, and mercury was over 3 times higher (Table 3). Thus, metal levels in roseate tern eggs on Long Island were relatively high, and the possibility of adverse reproductive effects requires scrutiny. To date there is no evidence of significant rates of infertility, embryonic mortality, or developmental defects for roseate terns (Gochfeld et al., 1997). Few studies report levels of selenium in bird eggs. King et al. (1983) and Ohlendorf and Harrison (1986) report levels from uncontaminated sites (Table 3) which are lower than we found for roseate eggs. Selenium levels from Franklin’s gull eggs in
TABLE 3 Levels of Metals in Eggs of Birds (ppb Adapted from Review by Burger, 1994)
Metal Cadmium Chromium Lead Manganesea Mercury Seleniumb
Number of studies or locations 26 10 25 2 44 2
Range of mean levels (ppb) 2—530 10—370 20—6700 500—4000 70—7290 300—2100
Mean level for all roseate eggs Median (1989—1994) 10 70 140 2250 33 1200
80 1100 1150 3540 1230 2310
Note. Given are ranges and median of the mean values (converted to ppb) as reported in a number of studies for each metal which vary geographically, taxonomically, and methodologically. a From Burger and Gochfeld, 1995, 1996. b From Ohlehdorf and Harrison, 1986; King et al., 1983.
Minnesota, however, averaged nearly 3 ppm (Burger and Gochfeld, 1996), which are higher than those reported here. Eggs from contaminated sites such as Kesterson in California, however, can have levels as high as 81 ppm which are grossly embryotoxic (Hoffman et al., 1988). Ohlendorf (1993) lists the toxic level as higher than 8 ppm. Thus, although the levels of selenium in roseate terns are at the high end for birds, they are not in the toxic range. Even fewer studies report manganese levels in eggs. We found mean levels of from 3 to 4 ppm for herring gulls in the same nesting area as the roseates in this study (Burger and Gochfeld, 1995). Long-Term Effects Roseate terns are a federally endangered species in the United States and Canada, and their populations have declined or remained stable while other closely related terns have not suffered. Although the causes of reproductive losses at any given colony are usually inclement weather, food shortage, or predators (Nisbet, 1980; Burger et al., 1995; Gochfeld et al., 1997), toxics may be a contributory factor. Toxics could interfere with fertility, reproductive behavior, embryonic development, chick maturation, or survival. This research was partly undertaken to determine if there were high levels of any metals in the eggs that might suggest possible developmental defects or lowered reproductive success, if there were increases in any metals over the period of decline, and if there were sufficiently high levels of any metals, compared to other local-nesting seabirds, to suggest that roseate terns may be more highly exposed and thus vulnerable. Nisbet (1993) found little direct evidence that the reproductive rate of seabirds has been impaired by heavy metals. Gochfeld (1980) attributed developmental defects in common terns of New York to elevated mercury levels. Hoffman et al. (1988) documented embryotoxicity of selenium in waterbirds in California. Mercury is particularly of interest because the lowest observed effect level (LOEL) from a variety of laboratory studies is about 1 ppm in eggs (Eisler, 1987; Burger, 1993). The mean levels of mercury in eggs of roseate terns were 1 ppm or higher for all six years, and it is during this period that the roseate terns decreased sharply in numbers. Although the proximate cause of lowered reproductive success was often predation, predation rates can be increased by a decrease in parental attentiveness and a decrease in chick nest site fidelity that can be affected by mercury. Although the harvesting of adult terns on the wintering grounds is likely to be the major factor
TEMPORAL TRENDS IN METALS IN ROSEATE TERN EGGS
affecting roseate tern populations (Gochfeld et al., 1997), the effects of pollutants may reduce hatching or chick survival, thereby preventing the population from compensating for the harvest. A 6-year period of annual sampling is not sufficient to detect long-term trends or cyclical fluctuations. Bioindicators such as the roseate tern eggs are valuable both for testing hypotheses about spatial and temporal trends or about remediation and for generating hypotheses as well. Although we have a convincing explanation for the increase followed by a decrease in the lead, chromium, and cadimium levels (1990—1992 vs 1993—1994), there is no comparable explanation for manganese and selenium. ACKNOWLEDGMENTS We thank I. C. T. Nisbet, H. Ohlendorf, and R. Furness for valuable discussions about toxicants; Robert Paxton and Sarah Plimpton and Carl Safina and Mercedes Lee for advice, logistical help, and accommodations over the years; and T. Shukla, J. Ondrof, R. Ramos, and T. Benson for laboratory analyses in the laboratory. Support for the analyses was provided by the U.S. Fish and Wildlife Service under a cooperative agreement; by NIEHS Grant ESO 5022; by the Consortium for Risk Evaluation with Stakeholder Participation (CRESP, Department of Energy AI No. DE-FC01-95EW55084); and by the Environmental and Occupational Health Sciences Institute. We thank the U.S. Fish and Wildlife Service and the New York State Department of Environmental Conservation for permits to collect specimens and conduct this research. Our procedures were approved by the Rutgers University Animal Review Board.
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