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Spatial and temporal patterns in metal levels in eggs of common terns (Sterna hirundo) in New Jersey
The Science of the Total Environment 311 (2003) 91–100
Spatial and temporal patterns in metal levels in eggs of common terns (Sterna hirundo) in New Jersey Joanna Burgera,b,*, Michael Gochfeldb,c a
Division of Life Sciences, 604 Allison Road, Rutgers University, Piscataway, NJ 08854-8082, USA b Environmental and Occupational Health Sciences Institute, Piscataway, NJ 08854, USA c Environmental and Community Medicine, UMDNJ-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA
Abstract Seabirds are excellent subjects for examination of metals because they feed at different trophic levels, including as top-level piscivores, they are long-lived, and many are abundant and widely distributed. In this paper we examine the levels of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in eggs from common terns (Sterna hirundo) nesting on five saltmarsh islands in Barnegat Bay, New Jersey from 2000 to 2002. We test the null hypothesis that there were no locational or temporal differences from 2000 to 2002. There were significant locational differences in all metals in some years, although the differences were not large. The levels of most metals do not seem sufficiently high to cause adverse effects, although the levels of mercury in eggs of some common terns from the bay are within the range known to cause adverse effects. Mercury in common tern eggs may be a contributing cause to their local decline. 䊚 2003 Elsevier Science B.V. All rights reserved. Keywords: Seabirds; Metals; Arsenic; Cadmium; Chromium; Lead; Manganese; Mercury; Selenium; Atlantic coast; Bioindicator
1. Introduction The public, managers and policy-makers are concerned about the levels of contaminants in our environment, and whether these levels are changing over time, reflecting either increased population, industrialization and pollution, or improved environmental controls. Natural levels of contaminants from geological and oceanic processes are augmented by anthropogenic sources from urban, industrial and agricultural emissions and effluents (Mailman, 1980). Local geological and anthropo*Corresponding author. Tel.: q1-732-445-4318; fax: q1732-445-5870. E-mail address: [email protected] (J. Burger).
genic sources are further enhanced by atmospheric transport and deposition (Fitzgerald, 1989). Once in aquatic environments, metals enter the food chain, and at each trophic level are either distributed among tissues or excreted (Lewis and Furness, 1991). With each step of the food chain, tissue concentrations increase, resulting in bioamplification. Top-level carnivores are often used as bioindicators because they are exposed to higher levels of contaminants than species that are lower on the food chain (Monteiro and Furness, 1995). Seabirds have been used as bioindicators of environmental contaminants because they are often top-level carnivores and are long-lived (Monteiro and Furness, 1995; Burger and Gochfeld, 2000).
0048-9697/03/$ - see front matter 䊚 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0048-9697(03)00135-9
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J. Burger, M. Gochfeld / The Science of the Total Environment 311 (2003) 91–100
In this paper we examine the levels of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in eggs from common terns (Sterna hirundo) nesting on five saltmarsh islands in Barnegat Bay, New Jersey, on the Atlantic coast of North America. We tested the null hypotheses that: (1) there were no locational differences in concentrations in eggs and (2) the levels of metals did not vary among years (2000–2002). We expected that there might be locational differences because previous work indicated that there were higher levels of contaminants in the northern end of the bay (Moser and Bopp, 2001). We did not expect yearly differences because, with only two inlets, there is little flushing and dilution capacity within the bay (Kennish, 2001c). The United Nations Group of Experts on Scientific Aspects of Marine Pollution noted that mercury, lead and cadmium are the most critical metal pollutants in marine waters (Fowler, 1990; Furness, 1996). Chemicals are often elevated in estuarine environments that receive direct input from large rivers and runoff from heavily urbanized environments. Although the margins of Barnegat Bay are neither highly industrialized nor urbanized, it is situated within the New York Bight (the coastal zone from Montauk, Long Island to Cape May, New Jersey), one of the most heavily contaminated estuarine regions in North America (NOAA, 1989; O’Connor and Ehler, 1991). Emissions and atmospheric transport of mercury brings a substantial load to the northeastern United States (NESCAUM, 1998). The recent United States national movement towards deregulation of energy production, beginning in 1999, has enhanced reliance on older, more polluting midwestern power plants (NJMTF, 2001), leading to increased emissions and atmospheric transport of contaminants, such as mercury, by prevailing winds from the Midwest to eastern states. As deregulation progresses, it is critical to have baseline information on contaminant levels to allow examination of temporal trends in the future. Most of a bird’s body burden of metals is obtained by ingestion (mainly from food rather than drinking water). A proportion of the ingested metal is absorbed from the gastrointestinal tract into the blood stream. The metals that circulate through
the body are deposited in various tissues or excreted. Different metals have affinity for different tissues. Metals can be sequestered in growing feathers or ‘excreted’ into the eggs of birds (Fimreite et al., 1982; Burger and Gochfeld, 1991a; Lewis and Furness, 1993; Gochfeld and Burger, 1998). Some metals are deposited in the eggshells as well (Burger, 1994). For some metals there is a positive correlation between metal levels in parents and their eggs (Burger and Gochfeld, 1991a, 1996). Developing embryos and newly hatched young are generally the stages most vulnerable to the effects of toxic substances (Burger and Gochfeld, 2000, 2001) and, conversely, eggs often represent local exposure of the adults that have laid them (Burger, 1993) and have been widely used as a bioindicator of pollution. The common tern is a widespread species, breeding throughout the Northern Hemisphere, and it has been extensively used in Europe as a bioindicator of environmental contamination (Becker et al., 1998). In North America, metal levels in tern eggs were measured as early as 1971 (Burger and Gochfeld, 1993). Since they eat almost exclusively fish, levels might be expected to be relatively high in their tissues and eggs. This affords the opportunity to examine temporal trends in metal levels, which is a critical need for environmental management (Rattner et al., 2000). This paper addresses this issue by examining levels of seven metals in eggs over a 3-year period. 2. Materials and methods The overall protocol was to determine if there were locational and temporal differences in levels of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in tern eggs within Barnegat Bay, in coastal New Jersey, from 2000 to 2002. Barnegat Bay (Fig. 1) ranges up to 6 km wide, and its shoreline is almost entirely developed, except for Island Beach State Park. The bay is mostly shallow, less than 2 m deep, with a very limited tidal fluctuation of less than 0.5 m. It is dotted with over 300 saltmarsh islands that vary in size and vegetation (Burger et al., 2001).
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Fig. 1. Map of New Jersey showing islands (shown in bold with and an asterisk) where terns nested.
In 1995 the Barnegat Bay–Little Egg Harbor estuarine ecosystem was designated the 28th National Estuary Program, and it is being studied extensively (Kennish, 2001a,b). In the 1900s (mostly between 1940 and 1970) 28% of the coastal wetlands in the system was lost to human development (Kennish, 2001c). The land surrounding the bay on the north, west and south is mostly suburban. The eastern boundary is a barrier island bordered by two inlets. Except for the 25-
mile-long Island Beach State Park, the beach is entirely developed with contiguous residential communities. The work was part of our long-term study of the population dynamics, breeding biology and ecotoxicology of colonial waterbirds in Barnegat Bay (Burger and Gochfeld, 1991b). Common terns have nested on up to 35 islands in the bay, although in any given year not all of these islands have been occupied (Burger and Gochfeld, 1991b).
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Table 1 Models explaining variation in metal levels in eggs of common terns in Barnegat Bay, NJ Model F P r2 Factors F(P) Year Location Year=location
Arsenic
Cadmium
Chromium
Manganese
9.46 (0.0001) 0.39
6.45 (0.0001) 0.30
3.8 (0.0001) 0.21
36.8 (0.0001) 0.71
33.4 (0.0001) 3.6 (0.008) NS
21.6 (0.0001) 5.4 (0.0004) NS
NS 6.7 (0.0001) 2.8 (0.02)
169.9 (0.0001) 6.0 (0.0002) NS
Mercury 6.5 (0.0001) 0.31 NS 13.4 (0.0001) 4.5 (0.0007)
Lead 6.4 (0.0001) 0.30 NS 5.64 (0.0003) 7.2 (0.0001)
Selenium 7.6 (0.0001) 0.34 19.7 (0.0001) 5.4 (0.0004) 4.1 (0.002)
NS, not significant (d.f.s11 164).
There has been a dramatic decline in the number of colonies over the last 20 years, from 30 colonies in 1977 to 14 in 1998 (Burger et al., 2001). All eggs were collected under appropriate state and federal collecting permits. To examine locational differences, eggs were collected from three– five islands each year, including Mike’s Island, Clam Island, Pettit Island, Marsh Elder and Sedge Island (Fig. 1). Terns move somewhat from year to year, based on the suitability of saltmarsh islands, making it difficult to compare islands directly (Burger and Gochfeld, 1991b). All samples were analyzed in the Elemental Laboratory at the Environmental and Occupational Health Sciences Institute in Piscataway, New Jersey. Whole egg contents were weighed, then dried in acid-washed weigh boats, and weighed again to obtain moisture content. The dried contents were individually digested in 70% nitric acid within microwave vessels for 10 min at 150 psi (10.6 kgycm2) and subsequently diluted with deionized water. Mercury was analyzed by the cold vapor technique, and other metals were analyzed by graphitefurnace atomic absorption. The mercury analysis was for total mercury, of which approximately 90% is assumed to be methylmercury (Lewis and Furness, 1993). All concentrations are expressed in nanograms per gram (ngyg or parts per billion) on a dry weight basis. Instrument detection limits were 0.02 ngyg for arsenic and cadmium, 0.08 ngyg for chromium, 0.15 ngyg for lead, 0.09 ngy g for manganese, 0.2 ngyg for mercury and 0.7
ngyg for selenium, but matrix detection limits were approximately one order of magnitude higher. All samples were run in batches that included a standard calibration curve and spiked samples. The acceptable recoveries on spiked specimens ranged from 85 to 115%. The acceptable coefficient of variation on replicate samples ranged up to 10%. We used stepwise multiple regression procedures on log-transformed data to determine the relative contribution of location, year and year=location to explain variance in each metal (PROC GLM, SAS, 1995). The procedure adds the variable that contributes the most to R 2, then adds the next variable that increases R 2 the most, continuing until all significant variables (Ps0.05) are added. Thus, variables that vary co-linearly are entered only if they add independently to explain the variation. The procedure also allows for categorical and interaction variables (year=location). We used the Duncan multiple range option with the ANOVA (SAS, 1995) as a post hoc test of the significance of the differences among means for the different islands. Both arithmetic and geometric means are given in Table 2 facilitate comparisons with other studies in the literature. 3. Results Regression analyses indicate that year was the most significant variable for arsenic, cadmium, manganese and selenium, while location was the variable that explained most of the variation for selenium, chromium and mercury (Table 1). The
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interaction of year=location was most significant for only lead. The data thus indicate that metal concentrations do not vary in the same manner for each metal. Although there are significant island andyor year differences (Table 1), the differences among islands or years were not great. For example, mean arsenic values varied only from 144 to 382 ngyg, chromium from 4 to 156 ngyg, and mercury from 698 to 2013 ngyg. The overall similarity in levels within metals suggests that means for Barnegat Bay would be useful for comparisons with other studies from elsewhere (see Fig. 1). There are, however, some patterns for some metals when viewed from a spatial context (Table 2 and Fig. 1). In Table 2, the islands are given from north (Mike’s Island) to the south (Sedge Island). Pattern differences include: (1) arsenic levels were highest at the northern end of the bay and the southern end; (2) cadmium, lead and manganese were highest in the lower half of the bay; (3) chromium and selenium were highest at the northern end of the bay; and (4) mercury was highest on Clam Island and Sedge Island, the islands closest to the inlets. When all the data are combined, there were some significant correlations among metals in eggs (Table 3), but the correlations are not high. The general lack of correlation indicates the metals are not co-varying. 4. Discussion Common terns normally return to their colonies in Barnegat Bay 3–4 weeks before egg-laying, and food obtained in this period is the main contributor of energy and nutrients in the eggs (Burger and Gochfeld, 1991b). The contaminants deposited in eggs reflect circulating levels in the blood at the time of egg-laying, which in turn reflects recent exposure much more than mobilization from body stores. Thus, even highly mobile species such as terns may serve as indicators of local exposure, even though the adults accumulate contaminants at their wintering grounds in South America, as well as at the breeding ground. The metals deposited in eggs mainly reflect local exposure (Burger and Gochfeld, 1993). While estab-
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lishing and defending territories, terns forage mainly within a few kilometers of their colonies, and hence would be exposed to local differences in metals in their prey fish in the few weeks prior to egg-laying (Burger and Gochfeld, 1991b). 4.1. Locational differences Although there were locational differences in metal levels, they were generally not great. Barnegat Bay is a long, thin bay with only two inlets, which limits the flushing and dilution capacity (Kennish, 2001c). Sediment analysis has shown higher levels of contaminants at the northern end of the bay than at the middle of the bay (cadmium, chromium, lead), due to past industrial activity in the north (Moser and Bopp, 2001); however, these authors did not take samples from the southern end of the bay. The relatively low flushing of the bay may result in lower turnover rates of the sediments, and thus lower dilution of chemicals that remain from contamination in the mid-1900s. In other systems, contaminant levels in fish (the primary food of common terns; Burger and Gochfeld, 1991b), are more highly related to those in sediment than either to surface or pore waters (SFWMD, 2001). Taken together, this led us to predict that contaminants in eggs from birds nesting in the north might be higher (Mike’s Island) than on the other islands, but this was the case only for arsenic in 2000, chromium and mercury. Common terns feed on a variety of fish, mainly in the 4–15-cm size range, and the availability of particular fish species varies locationally and temporally (Burger and Gochfeld, 1991b). Some of the terns’ favored prey fish species are localized, while others may be expected to move throughout the bay system. Moser and Bopp (2001) also reported higher lead levels in sediments near marinas, and there are fewer marinas in the southern part of the bay than in the north. Although none of the tern colonies examined within 1 km of marinas, lead levels were higher on Pettit and Marsh Elder, which are closest to the highest concentration of marinas. The variability among locations can also be partly explained by the fact that, depending on food availability, the terns from different colonies
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Table 2 Common tern eggs collected in 2000–2002 from Mike’s Island, Clam Island, Pettit Island, Marsh Elder and Sedge Island in Barnegat Bay, NJ Concentration (ngyg dry wt.) Mike’s Island Arsenic 2000 2001 2002 Cadmium 2000 2001 2002 Chromium 2000 2001 2002 Lead 2000 2001 2002 Manganese 2000 2001 2002 Mercury 2000 2001 2002 Selenium 2000
Wilcoxon (P)
Clam Island
Pettit Island
275"32 237 (A) 272"32 238 (A) 146"9 141 (B)
–
–
3"1 2 (A) 0.19"0.16 0.02 (C) 14"3 6 (A,B)
–
115"12 108 (A) 52"13 25 (A) 156"60 96 (A)
–
100"21 74 (B) 164"25 131 (A,B) 22"4 19 (B)
–
1860"224 1750 (B) 3997"415 3680 (B) 1640"100 1600 (B)
365"40 326 (A) 195"18 180 (A)
303"42 264 (A) 166"14 151 (A, B) –
1"0.3 0.2 (A,B) 10"1 8 (A,B)
0.36"0.12 0.08 (B,C) 5"1 4 (B) –
162"40 73 (B) 382"33 361 (A) 200"12 194 (A) 3"0.3 3 (A) 1.45"0.34 0.5 (A) 8"2 4 (A,B)
60"9 52 (A) 24"3 21 (B)
4"2 1 (B) 44"10 14 (A) 49"11 39 (B)
87"19 67 (B) 428"41 376 (A)
142"20 132 (A,B) 502"232 208 (A) 528"69 459 (A)
39"12 8 (A) 54"5 50 (B)
360"135 72 (A,B) 7"3 3 (B)
Marsh Elder
–
–
–
5180"489 4925 (A,B) 1594"94 1552 (B)
5750"396 5590 (A) 2040"108 2000 (A)
Sedge Island 144"27 78 (B) –
7 (0.02)
209"16 199 (A)
13 (0.0095)
6"2 4 (A)
7 (0.08)
NS 16 (0.0009)
– 17"5 7 (A)
9.5 (0.05)
14"3 6 (B)
25 (0.0001)
–
NS 47"6 40 (B)
248"63 173 (A) – 16"2 11 (B)
32 (-0.0001)
5 (0.07) 7 (0.08) 67.5 (-0.0001)
7 (0.03)
2660"278 2490 (A) 5200"274 5110 (A,B) 2020"127 1960 (A)
2380"178 2299 (A,B) –
2010"385 982 (A) – 1580"153 1473 (A)
15 (0.004)
1650"98
20 (0.0001)
1050"30 938 (A,B) 1090"117 980 (B) 999"81 948 (B)
–
–
1870"222 1570 (A) 977"130 851 (B)
847"83 798 (B) 1024"105 960 (B)
698"74 454 (B) 1070"128 993 (B) 1110"119 1020 (B)
2450"113
–
–
2030"90
1610"94 1563 (B)
12 (0.006) 14.7 (0.005)
8 (0.02) 11 (0.01)
J. Burger, M. Gochfeld / The Science of the Total Environment 311 (2003) 91–100
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Table 2 (Continued) Concentration (ngyg dry wt.)
2001 2002
Wilcoxon (P)
Mike’s Island
Clam Island
Pettit Island
Marsh Elder
Sedge Island
2420 (A) 2620"95 2600 (A) 2480"71 2470 (A)
2570"131 2510 (A) 2520"55 2520 (A)
2340"129 2300 (A) 2360"116 2290 (A)
2010 (B) 2650"58 2650 (A) 2480"83 2460 (A)
1600 (C) – 2520"77 (A)
NS NS
Results are given as arithmetic mean"S.E. Below are the geometric means with Duncan categories in parenthesis. Islands sharing a letter do not differ significantly. No terns nested on Clam or Pettit island in 2000 or on Sedge Island in 2001.
have to fly different distances to feeding grounds, sometimes in the bay itself and sometimes in inlets or over the ocean. Mercury was highest on Sedge Island in 2000 and 2002, and on Clam Island in 2001; both islands are the ones nearest to an ocean inlet where recreational fishing occurs and where there is regular influx of seawater. This has two implications: (1) mercury levels might be expected to be highest, since natural mercury is higher in seawater than in freshwater (Fowler, 1990); and (2) birds near an inlet often feed in nearby estuarine waters, in the inlet itself and in the nearby ocean (Burger and Gochfeld, 1991b). Common terns were observed to forage regularly at the inlet and offshore. Because of incomplete mixing, waters that are farthest from ocean inlets (i.e. near Pettit and Mike’s Island) might have lower mercury levels because they are diluted more by freshwater from small rivers and streams that empty into the bay than from the tide washing through the inlets. Table 3 Significant intermetal correlation (Kendall tau) of all common tern eggs (Ns176) collected from 2000 to 2001
Arsenic with:
Cadmium with: Chromium with:
Lead with:
Cadmium Manganese Mercury Selenium Manganese Lead Lead Manganese Selenium Manganese
r2
(P)
y0.21 0.20 0.18 0.17 y0.38 y0.12 y0.18 y0.12 0.13 0.18
0.0001 0.0001 0.004 0.0007 0.0001 0.02 0.0006 0.02 0.008 0.0002
Thus, birds foraging nearest to oceanic waters might be expected to have the highest levels of mercury, which was the case in this study. A similar pattern for mercury was noted for colonies in Barnegat Bay in 1995 (Burger and Gochfeld, 1997). Correlations among metals were not high, indicating that analysis of the levels of one metal will not provide insights into other metals. Correlations among metals might be expected to vary if concentrations in sediments vary among locations, as has been suggested for Barnegat Bay (Moser and Bopp, 2001). 4.2. Temporal trends While the examination of metals levels over long periods can provide insights into possible trends, short-term data sets (such as provided by this study) provide information that can be used to identify sudden shifts in contaminant levels, which might indicate a new point or non-point source of pollution. For point sources, a rapid increase in contaminants might be expected in only one local colony, while non-point sources might show up as a general increase throughout Barnegat Bay. Neither occurred for the tern eggs collected in Barnegat Bay from 2000 to 2002. Levels of arsenic, manganese, lead and selenium were highest in 2001 compared to the other years, suggesting that some event caused a general increase. Such an increase would be possible under several conditions, including increases in storm or boat activity that resulted in sediment disturbance. Since Barnegat Bay is so shallow (less than 2 m), severe storms can result in resuspension of sedi-
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ments (that could harbor metal contamination). The effects of such storms, or of increased boat activity, however, require additional study. 4.3. Potential adverse effects Concentrations of contaminants in tissues can be used as bioindicators of exposure and are useful in determining the trends in exposure. However, interpreting the biological significance of contaminant levels in eggs requires knowing the comparable levels that are associated (usually experimentally) with adverse effects. Such information comes from laboratory studies (Eisler, 1985a,b, 1986, 1988). More data are available for mercury (Burger and Gochfeld, 1997) than for the other metals. Many laboratory studies give dose and effects, but do not examine tissue levels (Burger and Gochfeld, 1997, 2001). Conversely, field studies may yield tissue or egg levels without being linked to effects. Another method of evaluating effects is to compare the levels found in a target population with those normally occurring in similar species of birds, in this case several taxa of fish-eating birds, that do not seem to be adversely affected (Burger and Gochfeld, 2001). It is likely that if the levels found in eggs from a particular region are not above the median for a wide range of piscivorous species, the birds are not adversely affected. Using this method, the eggs of common terns nesting in Barnegat Bay are probably not affected by cadmium (median of 12 ngyg for fish-eating birds, and 4 ngyg for Barnegat Bay common terns, after Burger 2002). Similar comparisons are: chromium, 210 vs. 45 ngyg for Barnegat terns; and lead, 190 vs. 163 ngyg (after Burger, 2002). Remarkably few studies have examined levels of arsenic, and even the Eisler (1994) review did not report any effects studies for arsenic levels in eggs. However, the mean levels of three elements were higher in the eggs of common terns from Barnegat Bay than the median for a wide range of fish-eating birds: manganese, 510 ngyg for a range of fish-eating birds vs. 2898 ngyg for Barnegat common terns; mercury, 340 vs. 1194 ngyg; and selenium, 1100 vs. 2420 ngyg (after Burger,
2002). This suggests that these three elements bear further examination. The relationship between levels in eggs and adverse developmental effects is known for mercury (Eisler, 1987). Adverse effects, including mortality, lowered hatching rates, higher chick defects and other neurobehavioral deficits, can occur when eggs levels are as low as 500 ngyg (wet weight), and more severe effects usually occur at 1000–2000 ngyg (Eisler, 1987). Thus, the levels of mercury in eggs of common terns from Barnegat Bay appear to be within the range that might cause neurobehavioral effects. Moreover, when the egg data are examined by location, the mercury levels at Sedge Island, nearest the Little Egg Harbor Inlet, averaged 2010 ngyg. The number of common tern colonies has been declining in Barnegat Bay over the last 20 years (Burger et al., 2001). Terns that are consistently unsuccessful at raising young tend to move to other colony sites in future years. If contaminant burdens contribute to low reproductive success locally, they would be a contributing factor to regional population declines. Manganese is an essential micronutrient that is an important cofactor in metabolism (Drown et al., 1986). At high doses it is toxic. In laboratory studies, excess manganese exposure causes mortality and decreased fertility (Gray and Laskey, 1980; Laskey et al., 1982), decreases in motor activity (Ingersoll et al., 1995), learning disabilities (Senturk and Oner, 1996), and nervous system dysfunction and convulsions (Mergler, 1986). In birds, manganese causes neurobehavioral defects, similar in nature to those caused by lead (Burger and Gochfeld, 1995, 2001). Unfortunately, the levels of manganese in eggs associated with these adverse effects in chicks have not yet been determined. Selenium levels in the eggs of common terns were also above the median for other fish-eating birds (Burger, 2002), but field studies (see below) suggest that they are not at a level of concern. Selenium levels can be sufficiently high to cause adverse effects in birds (Heinz, 1996), and levels as high as 81 000 ngyg caused adverse effects in birds at Kesterson Reservoir in California (Hoffman et al., 1988). Ohlendorf et al. (1986) showed
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that adverse reproductive effects occur at approximately 10 000 ngyg of selenium in eggs, while Heinz (1996) reported that adverse reproductive effects can occur at selenium concentrations as low as 3000 ngyg (wet weight) in eggs. The levels of selenium in tern eggs from Barnegat Bay were lower (mean of 2040 ngyg). Furthermore, the levels of selenium that King et al. (1983) found in bird eggs from an uncontaminated site in Texas were similar to those of the tern eggs from Barnegat Bay. 5. Conclusions The results of this study indicate that although there are locational differences in metal levels for eggs collected from the colonies in Barnegat Bay, the differences were not great. However, mercury levels were highest nearest to an ocean inlet. Furthermore, although significant, the yearly variations were not great. The 3 years of data indicate that contaminant data from only two of these years are insufficient to determine trends, since had we used only the first 2 years we would have concluded that there were significant increases in several metals, when in fact the levels were lower in the third year. The levels of most metals do not seem sufficiently high to cause adverse effects, although the levels of mercury in eggs of some common terns from the bay are within the range known to cause adverse effects. Acknowledgments We thank R. Furness, I.C.T. Nisbet, H.M. Ohlendorf, and D. Peakall for valuable discussions about metals in seabirds; K. Cooper, M. Gallo, B.D. Goldstein and C. Powers for discussion about risk assessment; Fred Lesser for logistical help over the years; T. Shukia and C. Dixon for assistance in the laboratory; and R. Ramos for graphics. Support for the analyses was provided by the New York Bioscape Program (Wildlife Trust) and NIEHS grant ESO 5022. Research on the colonial birds in Barnegat Bay is conducted under the auspices of the Endangered and Non-Game Species Program of the New Jersey Department of Environmental Protection, and the US Environ-
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mental Protection Agency. We thank the US Fish and Wildlife Service and New Jersey Department of Environmental Protection for permits to collect specimens and conduct this research. All procedures and protocols were approved by the Rutgers University Animal Review Board. References Becker PH, Thyen S, Mickstein S, Sommer U, Schmieder KR. Monitoring pollutants in coastal bird eggs in the Wadden Sea. Wadden Sea Ecosystem No 8. Germany: Wilhelmshaven, 1998. Burger J. Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 1993;5:203 –311. Burger J. Heavy metals in avian eggshells: another excretion method. J Toxicol Environ Health 1994;41:253 –258. Burger J. Food chain differences affect heavy metals in birds in Barnegat Bay, New Jersey. Environ Res 2002;90:33 –39. Burger J, Gochfeld M. Cadmium and lead in common terns (Aves, Sterna hirundo): relationship between levels in parents and eggs. Environ Monit Assess 1991;16:253 –258. Burger J, Gochfeld M. The common tern: breeding biology and behavior. New York: Columbia University Press, 1991. Burger J, Gochfeld M. Lead and cadmium accumulation in eggs and fledgling seabirds in the New York Bight. Environ Toxicol Chem 1993;12:261 –267. Burger J, Gochfeld M. Growth and behavioral effects of early postnatal chromium and manganese exposure in herring gull (Larus argentatus) chicks. Pharmacol Biochem Behav 1995;50:607 –612. Burger J, Gochfeld M. Heavy metal and selenium levels in Franklin’s gull (Larus pipixcan) parents and their eggs. Archiv Environ Contam Toxicol 1996;30:481 –487. Burger J, Gochfeld M. Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ Res 1997;75:160 –172. Burger J, Gochfeld M. Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health B 2000;3:59 –78. Burger J, Gochfeld M. Effects of chemicals and pollution on seabirds. In: Schreiber EA, Burger J, editors. Biology of marine birds. Boca Raton, FL: CRC Press, 2001. p. 485 – 525. Burger J, Jenkins CD, Lesser F, Gochfeld M. Population trends of colonially nesting birds in Barnegat Bay. J Coastal Res 2001;32:197 –211. Special issue. Drown DB, Oberg SG, Sharma RP. Pulmonary clearance of soluble and insoluble forms of manganese. J Toxicol Environ Health 1986;17:201 –212. Eisler R. Selenium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service Biology Report 85 (噛1.5) 1985. Eisler R. Cadmium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service Biology Report 85 (噛1.2). 1985.
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Eisler R. Chromium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service Biology Report 85 (噛1.6). 1986. Eisler R. Mercury hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service Biology Report 85 (噛1.1). 1987. Eisler R. Lead hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service Biology Report 85 (噛1.14) 1988. Eisler R. A review of arsenic hazards to plants and animals with emphasis on fishery and wildlife resources. In: Nriagu JO, editor. Arsenic in the environment. Part 11: human health and ecosystem effects. New York: Wiley & Sons, 1994. p. 185 –258. Fimreite N, Brevik F, Trop R. Mercury and organochlorines in eggs from a Norwegian gannet colony. Arch Environ Contam Toxicol 1982;28:58 –60. Fitzgerald WF. Atmospheric and oceanic cycling of mercury. In: Riley JP, Chester R, editors. Chemical oceanography, vol. 10. New York: Academic Press, 1989. p. 151 –186. Fowler SW. Critical review of selected heavy metal and chlorinated hydrocarbon concentrations in the marine environment. Mar Environ Res 1990;29:1 –64. Furness RW. Cadmium in birds. In: Beyer WN, Heinz GH, Redmom-Norwood AW, editors. Environmental contaminants in wildlife: interpreting tissue concentrations. Boca Raton, FL: Lewis Press, 1996. p. 389 –404. Gochfeld M, Burger J. Temporal trends in metal levels in eggs of the endangered roseate tern (Sterna dougallin) in New York. Environ Res 1998;77:36 –42. Gray LE Jr, Laskey JW. Multivariate analysis of the effects of manganese on the reproductive physiology and behavior of the male house mouse. J Toxicol Environ Health 1980;6:861 –867. Heinz GH. Selenium in birds. In: Beyer WN, Heinz GH, Redmom-Norwood AW, editors. Environmental contaminants in wildlife: interpreting tissue concentrations. Boca Raton, FL: Lewis, 1996. p. 447 –458. Hoffman DJ, Ohlendorf HM, Aldrich TW. Selenium teratogenesis in natural populations of aquatic birds in central California. Arch Environ Contam Toxicol 1988;17:519 –525. Ingersoll RT, Montgomery EB Jr, Aposhian HV. Central system toxicity of manganese. Fund Appl Toxicol 1995;27:106 – 113. Kennish M, editor. Barnegat Bay–Little Egg Harbor, New Jersey: estuary and watershed assessment wspecial issuex. J Coastal Res, 2001a;32:3–280. Kennish M. Characterization of the Barnegat Bay–Little Egg Harbor estuary and watershed. J Coastal Res 2001b;32:3 – 12. Kennish M. State of the estuary and watershed: an overview. J Coastal Res 2001c;32:243 –273. King KA, Lefever CA, Mulhern BM. Organochlorine and metal levels in royal terns nesting on the central Texas coast. J Field Ornithol 1983;54:295 –303.
Laskey JW, Rehnberg GL, Hein JF, Carter SD. Effects of chronic manganese (Mg3O4) exposure on selected reproductive parameters in rats. J Toxicol Environ Health 1982;9:677 –687. Lewis SA, Furness RW. Mercury accumulation and excretion by laboratory-reared black-headed gulls (Larus ridibundus) chicks. Arch Environ Contam Toxicol 1991;21:316 –320. Lewis SA, Furness RW. The role of eggs in mercury excretion by quail Coturnix coturnix and the implications for monitoring mercury pollution by analysis of feathers. Ecotoxicology 1993;2:55 –64. Mailman RB. Heavy metals. In: Perry JJ, editor. Introduction to environmental toxicology. New York: Elsevier, 1980. p. 34 –43. Mergler D. Manganese: the controversial metal. At what levels can deleterious effects occur? Can J Neurol Sci 1986;23:93 – 94. Monteiro LR, Furness RW. Seabirds as monitors of mercury in the marine environment. Water Air Soil Pollut 1995;80:831 –870. Moser FC, Bopp R. Particle-associated contaminants in the Barnegat Bay–Little Egg Harbor Estuary. J Coastal Res 2001;32:229 –243. Special issue. NESCAUM. Atmospheric mercury emissions in the northeastern states. Boston, MA: Northeast States for Coordinated Air Use Management (NESCAUM), 1998. NJMTF. Mercury in New Jersey. Report of the Task Force, vols. 1–3. Trenton, NJ: New Jersey Mercury Task Force, New Jersey Department of Environmental Protection, 2001. Oaa N. A summary of data on tissue contamination from the first three years (1986–1988) of the mussel watch program. Technical Memorandum NOS OMA 49. Rockville, MD: National Oceanographic and Atmospheric Administration, 1989. O’Connor TP, Ehler CN. Results from the NOAA National Status and Trends Program on distribution and effects of chemical contamination in the coastal and estuarine United States. Environ Monitor Assess 1991;17:33 –49. Ohlendorf HM, Hothem RL, Bunck CM, Aldrich TW, Moore JF. Relationships between selenium concentrations and avian reproduction. Trans N Am Wildl Nat Resour Conf 1986;51:330 –342. Rattner BA, Pearson JL, Golden NH, Cohen JB, Erwin RM, Ottinger MA. Contaminant exposure and effects—terrestrial vertebrates database: trends and data gaps for Atlantic coast estuaries. Environ Monit Assess 2000;63:131 –142. SAS. SAS User’s Guide. Cary, NC: Statistical Analysis Institute, 1995. Senturk UK, Oner G. The effect of manganese-induced hypercholesterolemia on learning in rats. Biol Trace Elem Res 1996;51:249 –257. SFWMD. Everglades consolidated report. Fort Lauderdale, FL: South Florida Water Management District, 2001.
Spatial and temporal patterns in metal levels in eggs of common terns (Sterna hirundo) in New Jersey Joanna Burgera,b,*, Michael Gochfeldb,c a
Division of Life Sciences, 604 Allison Road, Rutgers University, Piscataway, NJ 08854-8082, USA b Environmental and Occupational Health Sciences Institute, Piscataway, NJ 08854, USA c Environmental and Community Medicine, UMDNJ-Robert Wood Johnson Medical School, Piscataway, NJ 08854, USA
Abstract Seabirds are excellent subjects for examination of metals because they feed at different trophic levels, including as top-level piscivores, they are long-lived, and many are abundant and widely distributed. In this paper we examine the levels of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in eggs from common terns (Sterna hirundo) nesting on five saltmarsh islands in Barnegat Bay, New Jersey from 2000 to 2002. We test the null hypothesis that there were no locational or temporal differences from 2000 to 2002. There were significant locational differences in all metals in some years, although the differences were not large. The levels of most metals do not seem sufficiently high to cause adverse effects, although the levels of mercury in eggs of some common terns from the bay are within the range known to cause adverse effects. Mercury in common tern eggs may be a contributing cause to their local decline. 䊚 2003 Elsevier Science B.V. All rights reserved. Keywords: Seabirds; Metals; Arsenic; Cadmium; Chromium; Lead; Manganese; Mercury; Selenium; Atlantic coast; Bioindicator
1. Introduction The public, managers and policy-makers are concerned about the levels of contaminants in our environment, and whether these levels are changing over time, reflecting either increased population, industrialization and pollution, or improved environmental controls. Natural levels of contaminants from geological and oceanic processes are augmented by anthropogenic sources from urban, industrial and agricultural emissions and effluents (Mailman, 1980). Local geological and anthropo*Corresponding author. Tel.: q1-732-445-4318; fax: q1732-445-5870. E-mail address: [email protected] (J. Burger).
genic sources are further enhanced by atmospheric transport and deposition (Fitzgerald, 1989). Once in aquatic environments, metals enter the food chain, and at each trophic level are either distributed among tissues or excreted (Lewis and Furness, 1991). With each step of the food chain, tissue concentrations increase, resulting in bioamplification. Top-level carnivores are often used as bioindicators because they are exposed to higher levels of contaminants than species that are lower on the food chain (Monteiro and Furness, 1995). Seabirds have been used as bioindicators of environmental contaminants because they are often top-level carnivores and are long-lived (Monteiro and Furness, 1995; Burger and Gochfeld, 2000).
0048-9697/03/$ - see front matter 䊚 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0048-9697(03)00135-9
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In this paper we examine the levels of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in eggs from common terns (Sterna hirundo) nesting on five saltmarsh islands in Barnegat Bay, New Jersey, on the Atlantic coast of North America. We tested the null hypotheses that: (1) there were no locational differences in concentrations in eggs and (2) the levels of metals did not vary among years (2000–2002). We expected that there might be locational differences because previous work indicated that there were higher levels of contaminants in the northern end of the bay (Moser and Bopp, 2001). We did not expect yearly differences because, with only two inlets, there is little flushing and dilution capacity within the bay (Kennish, 2001c). The United Nations Group of Experts on Scientific Aspects of Marine Pollution noted that mercury, lead and cadmium are the most critical metal pollutants in marine waters (Fowler, 1990; Furness, 1996). Chemicals are often elevated in estuarine environments that receive direct input from large rivers and runoff from heavily urbanized environments. Although the margins of Barnegat Bay are neither highly industrialized nor urbanized, it is situated within the New York Bight (the coastal zone from Montauk, Long Island to Cape May, New Jersey), one of the most heavily contaminated estuarine regions in North America (NOAA, 1989; O’Connor and Ehler, 1991). Emissions and atmospheric transport of mercury brings a substantial load to the northeastern United States (NESCAUM, 1998). The recent United States national movement towards deregulation of energy production, beginning in 1999, has enhanced reliance on older, more polluting midwestern power plants (NJMTF, 2001), leading to increased emissions and atmospheric transport of contaminants, such as mercury, by prevailing winds from the Midwest to eastern states. As deregulation progresses, it is critical to have baseline information on contaminant levels to allow examination of temporal trends in the future. Most of a bird’s body burden of metals is obtained by ingestion (mainly from food rather than drinking water). A proportion of the ingested metal is absorbed from the gastrointestinal tract into the blood stream. The metals that circulate through
the body are deposited in various tissues or excreted. Different metals have affinity for different tissues. Metals can be sequestered in growing feathers or ‘excreted’ into the eggs of birds (Fimreite et al., 1982; Burger and Gochfeld, 1991a; Lewis and Furness, 1993; Gochfeld and Burger, 1998). Some metals are deposited in the eggshells as well (Burger, 1994). For some metals there is a positive correlation between metal levels in parents and their eggs (Burger and Gochfeld, 1991a, 1996). Developing embryos and newly hatched young are generally the stages most vulnerable to the effects of toxic substances (Burger and Gochfeld, 2000, 2001) and, conversely, eggs often represent local exposure of the adults that have laid them (Burger, 1993) and have been widely used as a bioindicator of pollution. The common tern is a widespread species, breeding throughout the Northern Hemisphere, and it has been extensively used in Europe as a bioindicator of environmental contamination (Becker et al., 1998). In North America, metal levels in tern eggs were measured as early as 1971 (Burger and Gochfeld, 1993). Since they eat almost exclusively fish, levels might be expected to be relatively high in their tissues and eggs. This affords the opportunity to examine temporal trends in metal levels, which is a critical need for environmental management (Rattner et al., 2000). This paper addresses this issue by examining levels of seven metals in eggs over a 3-year period. 2. Materials and methods The overall protocol was to determine if there were locational and temporal differences in levels of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in tern eggs within Barnegat Bay, in coastal New Jersey, from 2000 to 2002. Barnegat Bay (Fig. 1) ranges up to 6 km wide, and its shoreline is almost entirely developed, except for Island Beach State Park. The bay is mostly shallow, less than 2 m deep, with a very limited tidal fluctuation of less than 0.5 m. It is dotted with over 300 saltmarsh islands that vary in size and vegetation (Burger et al., 2001).
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Fig. 1. Map of New Jersey showing islands (shown in bold with and an asterisk) where terns nested.
In 1995 the Barnegat Bay–Little Egg Harbor estuarine ecosystem was designated the 28th National Estuary Program, and it is being studied extensively (Kennish, 2001a,b). In the 1900s (mostly between 1940 and 1970) 28% of the coastal wetlands in the system was lost to human development (Kennish, 2001c). The land surrounding the bay on the north, west and south is mostly suburban. The eastern boundary is a barrier island bordered by two inlets. Except for the 25-
mile-long Island Beach State Park, the beach is entirely developed with contiguous residential communities. The work was part of our long-term study of the population dynamics, breeding biology and ecotoxicology of colonial waterbirds in Barnegat Bay (Burger and Gochfeld, 1991b). Common terns have nested on up to 35 islands in the bay, although in any given year not all of these islands have been occupied (Burger and Gochfeld, 1991b).
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Table 1 Models explaining variation in metal levels in eggs of common terns in Barnegat Bay, NJ Model F P r2 Factors F(P) Year Location Year=location
Arsenic
Cadmium
Chromium
Manganese
9.46 (0.0001) 0.39
6.45 (0.0001) 0.30
3.8 (0.0001) 0.21
36.8 (0.0001) 0.71
33.4 (0.0001) 3.6 (0.008) NS
21.6 (0.0001) 5.4 (0.0004) NS
NS 6.7 (0.0001) 2.8 (0.02)
169.9 (0.0001) 6.0 (0.0002) NS
Mercury 6.5 (0.0001) 0.31 NS 13.4 (0.0001) 4.5 (0.0007)
Lead 6.4 (0.0001) 0.30 NS 5.64 (0.0003) 7.2 (0.0001)
Selenium 7.6 (0.0001) 0.34 19.7 (0.0001) 5.4 (0.0004) 4.1 (0.002)
NS, not significant (d.f.s11 164).
There has been a dramatic decline in the number of colonies over the last 20 years, from 30 colonies in 1977 to 14 in 1998 (Burger et al., 2001). All eggs were collected under appropriate state and federal collecting permits. To examine locational differences, eggs were collected from three– five islands each year, including Mike’s Island, Clam Island, Pettit Island, Marsh Elder and Sedge Island (Fig. 1). Terns move somewhat from year to year, based on the suitability of saltmarsh islands, making it difficult to compare islands directly (Burger and Gochfeld, 1991b). All samples were analyzed in the Elemental Laboratory at the Environmental and Occupational Health Sciences Institute in Piscataway, New Jersey. Whole egg contents were weighed, then dried in acid-washed weigh boats, and weighed again to obtain moisture content. The dried contents were individually digested in 70% nitric acid within microwave vessels for 10 min at 150 psi (10.6 kgycm2) and subsequently diluted with deionized water. Mercury was analyzed by the cold vapor technique, and other metals were analyzed by graphitefurnace atomic absorption. The mercury analysis was for total mercury, of which approximately 90% is assumed to be methylmercury (Lewis and Furness, 1993). All concentrations are expressed in nanograms per gram (ngyg or parts per billion) on a dry weight basis. Instrument detection limits were 0.02 ngyg for arsenic and cadmium, 0.08 ngyg for chromium, 0.15 ngyg for lead, 0.09 ngy g for manganese, 0.2 ngyg for mercury and 0.7
ngyg for selenium, but matrix detection limits were approximately one order of magnitude higher. All samples were run in batches that included a standard calibration curve and spiked samples. The acceptable recoveries on spiked specimens ranged from 85 to 115%. The acceptable coefficient of variation on replicate samples ranged up to 10%. We used stepwise multiple regression procedures on log-transformed data to determine the relative contribution of location, year and year=location to explain variance in each metal (PROC GLM, SAS, 1995). The procedure adds the variable that contributes the most to R 2, then adds the next variable that increases R 2 the most, continuing until all significant variables (Ps0.05) are added. Thus, variables that vary co-linearly are entered only if they add independently to explain the variation. The procedure also allows for categorical and interaction variables (year=location). We used the Duncan multiple range option with the ANOVA (SAS, 1995) as a post hoc test of the significance of the differences among means for the different islands. Both arithmetic and geometric means are given in Table 2 facilitate comparisons with other studies in the literature. 3. Results Regression analyses indicate that year was the most significant variable for arsenic, cadmium, manganese and selenium, while location was the variable that explained most of the variation for selenium, chromium and mercury (Table 1). The
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interaction of year=location was most significant for only lead. The data thus indicate that metal concentrations do not vary in the same manner for each metal. Although there are significant island andyor year differences (Table 1), the differences among islands or years were not great. For example, mean arsenic values varied only from 144 to 382 ngyg, chromium from 4 to 156 ngyg, and mercury from 698 to 2013 ngyg. The overall similarity in levels within metals suggests that means for Barnegat Bay would be useful for comparisons with other studies from elsewhere (see Fig. 1). There are, however, some patterns for some metals when viewed from a spatial context (Table 2 and Fig. 1). In Table 2, the islands are given from north (Mike’s Island) to the south (Sedge Island). Pattern differences include: (1) arsenic levels were highest at the northern end of the bay and the southern end; (2) cadmium, lead and manganese were highest in the lower half of the bay; (3) chromium and selenium were highest at the northern end of the bay; and (4) mercury was highest on Clam Island and Sedge Island, the islands closest to the inlets. When all the data are combined, there were some significant correlations among metals in eggs (Table 3), but the correlations are not high. The general lack of correlation indicates the metals are not co-varying. 4. Discussion Common terns normally return to their colonies in Barnegat Bay 3–4 weeks before egg-laying, and food obtained in this period is the main contributor of energy and nutrients in the eggs (Burger and Gochfeld, 1991b). The contaminants deposited in eggs reflect circulating levels in the blood at the time of egg-laying, which in turn reflects recent exposure much more than mobilization from body stores. Thus, even highly mobile species such as terns may serve as indicators of local exposure, even though the adults accumulate contaminants at their wintering grounds in South America, as well as at the breeding ground. The metals deposited in eggs mainly reflect local exposure (Burger and Gochfeld, 1993). While estab-
95
lishing and defending territories, terns forage mainly within a few kilometers of their colonies, and hence would be exposed to local differences in metals in their prey fish in the few weeks prior to egg-laying (Burger and Gochfeld, 1991b). 4.1. Locational differences Although there were locational differences in metal levels, they were generally not great. Barnegat Bay is a long, thin bay with only two inlets, which limits the flushing and dilution capacity (Kennish, 2001c). Sediment analysis has shown higher levels of contaminants at the northern end of the bay than at the middle of the bay (cadmium, chromium, lead), due to past industrial activity in the north (Moser and Bopp, 2001); however, these authors did not take samples from the southern end of the bay. The relatively low flushing of the bay may result in lower turnover rates of the sediments, and thus lower dilution of chemicals that remain from contamination in the mid-1900s. In other systems, contaminant levels in fish (the primary food of common terns; Burger and Gochfeld, 1991b), are more highly related to those in sediment than either to surface or pore waters (SFWMD, 2001). Taken together, this led us to predict that contaminants in eggs from birds nesting in the north might be higher (Mike’s Island) than on the other islands, but this was the case only for arsenic in 2000, chromium and mercury. Common terns feed on a variety of fish, mainly in the 4–15-cm size range, and the availability of particular fish species varies locationally and temporally (Burger and Gochfeld, 1991b). Some of the terns’ favored prey fish species are localized, while others may be expected to move throughout the bay system. Moser and Bopp (2001) also reported higher lead levels in sediments near marinas, and there are fewer marinas in the southern part of the bay than in the north. Although none of the tern colonies examined within 1 km of marinas, lead levels were higher on Pettit and Marsh Elder, which are closest to the highest concentration of marinas. The variability among locations can also be partly explained by the fact that, depending on food availability, the terns from different colonies
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Table 2 Common tern eggs collected in 2000–2002 from Mike’s Island, Clam Island, Pettit Island, Marsh Elder and Sedge Island in Barnegat Bay, NJ Concentration (ngyg dry wt.) Mike’s Island Arsenic 2000 2001 2002 Cadmium 2000 2001 2002 Chromium 2000 2001 2002 Lead 2000 2001 2002 Manganese 2000 2001 2002 Mercury 2000 2001 2002 Selenium 2000
Wilcoxon (P)
Clam Island
Pettit Island
275"32 237 (A) 272"32 238 (A) 146"9 141 (B)
–
–
3"1 2 (A) 0.19"0.16 0.02 (C) 14"3 6 (A,B)
–
115"12 108 (A) 52"13 25 (A) 156"60 96 (A)
–
100"21 74 (B) 164"25 131 (A,B) 22"4 19 (B)
–
1860"224 1750 (B) 3997"415 3680 (B) 1640"100 1600 (B)
365"40 326 (A) 195"18 180 (A)
303"42 264 (A) 166"14 151 (A, B) –
1"0.3 0.2 (A,B) 10"1 8 (A,B)
0.36"0.12 0.08 (B,C) 5"1 4 (B) –
162"40 73 (B) 382"33 361 (A) 200"12 194 (A) 3"0.3 3 (A) 1.45"0.34 0.5 (A) 8"2 4 (A,B)
60"9 52 (A) 24"3 21 (B)
4"2 1 (B) 44"10 14 (A) 49"11 39 (B)
87"19 67 (B) 428"41 376 (A)
142"20 132 (A,B) 502"232 208 (A) 528"69 459 (A)
39"12 8 (A) 54"5 50 (B)
360"135 72 (A,B) 7"3 3 (B)
Marsh Elder
–
–
–
5180"489 4925 (A,B) 1594"94 1552 (B)
5750"396 5590 (A) 2040"108 2000 (A)
Sedge Island 144"27 78 (B) –
7 (0.02)
209"16 199 (A)
13 (0.0095)
6"2 4 (A)
7 (0.08)
NS 16 (0.0009)
– 17"5 7 (A)
9.5 (0.05)
14"3 6 (B)
25 (0.0001)
–
NS 47"6 40 (B)
248"63 173 (A) – 16"2 11 (B)
32 (-0.0001)
5 (0.07) 7 (0.08) 67.5 (-0.0001)
7 (0.03)
2660"278 2490 (A) 5200"274 5110 (A,B) 2020"127 1960 (A)
2380"178 2299 (A,B) –
2010"385 982 (A) – 1580"153 1473 (A)
15 (0.004)
1650"98
20 (0.0001)
1050"30 938 (A,B) 1090"117 980 (B) 999"81 948 (B)
–
–
1870"222 1570 (A) 977"130 851 (B)
847"83 798 (B) 1024"105 960 (B)
698"74 454 (B) 1070"128 993 (B) 1110"119 1020 (B)
2450"113
–
–
2030"90
1610"94 1563 (B)
12 (0.006) 14.7 (0.005)
8 (0.02) 11 (0.01)
J. Burger, M. Gochfeld / The Science of the Total Environment 311 (2003) 91–100
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Table 2 (Continued) Concentration (ngyg dry wt.)
2001 2002
Wilcoxon (P)
Mike’s Island
Clam Island
Pettit Island
Marsh Elder
Sedge Island
2420 (A) 2620"95 2600 (A) 2480"71 2470 (A)
2570"131 2510 (A) 2520"55 2520 (A)
2340"129 2300 (A) 2360"116 2290 (A)
2010 (B) 2650"58 2650 (A) 2480"83 2460 (A)
1600 (C) – 2520"77 (A)
NS NS
Results are given as arithmetic mean"S.E. Below are the geometric means with Duncan categories in parenthesis. Islands sharing a letter do not differ significantly. No terns nested on Clam or Pettit island in 2000 or on Sedge Island in 2001.
have to fly different distances to feeding grounds, sometimes in the bay itself and sometimes in inlets or over the ocean. Mercury was highest on Sedge Island in 2000 and 2002, and on Clam Island in 2001; both islands are the ones nearest to an ocean inlet where recreational fishing occurs and where there is regular influx of seawater. This has two implications: (1) mercury levels might be expected to be highest, since natural mercury is higher in seawater than in freshwater (Fowler, 1990); and (2) birds near an inlet often feed in nearby estuarine waters, in the inlet itself and in the nearby ocean (Burger and Gochfeld, 1991b). Common terns were observed to forage regularly at the inlet and offshore. Because of incomplete mixing, waters that are farthest from ocean inlets (i.e. near Pettit and Mike’s Island) might have lower mercury levels because they are diluted more by freshwater from small rivers and streams that empty into the bay than from the tide washing through the inlets. Table 3 Significant intermetal correlation (Kendall tau) of all common tern eggs (Ns176) collected from 2000 to 2001
Arsenic with:
Cadmium with: Chromium with:
Lead with:
Cadmium Manganese Mercury Selenium Manganese Lead Lead Manganese Selenium Manganese
r2
(P)
y0.21 0.20 0.18 0.17 y0.38 y0.12 y0.18 y0.12 0.13 0.18
0.0001 0.0001 0.004 0.0007 0.0001 0.02 0.0006 0.02 0.008 0.0002
Thus, birds foraging nearest to oceanic waters might be expected to have the highest levels of mercury, which was the case in this study. A similar pattern for mercury was noted for colonies in Barnegat Bay in 1995 (Burger and Gochfeld, 1997). Correlations among metals were not high, indicating that analysis of the levels of one metal will not provide insights into other metals. Correlations among metals might be expected to vary if concentrations in sediments vary among locations, as has been suggested for Barnegat Bay (Moser and Bopp, 2001). 4.2. Temporal trends While the examination of metals levels over long periods can provide insights into possible trends, short-term data sets (such as provided by this study) provide information that can be used to identify sudden shifts in contaminant levels, which might indicate a new point or non-point source of pollution. For point sources, a rapid increase in contaminants might be expected in only one local colony, while non-point sources might show up as a general increase throughout Barnegat Bay. Neither occurred for the tern eggs collected in Barnegat Bay from 2000 to 2002. Levels of arsenic, manganese, lead and selenium were highest in 2001 compared to the other years, suggesting that some event caused a general increase. Such an increase would be possible under several conditions, including increases in storm or boat activity that resulted in sediment disturbance. Since Barnegat Bay is so shallow (less than 2 m), severe storms can result in resuspension of sedi-
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ments (that could harbor metal contamination). The effects of such storms, or of increased boat activity, however, require additional study. 4.3. Potential adverse effects Concentrations of contaminants in tissues can be used as bioindicators of exposure and are useful in determining the trends in exposure. However, interpreting the biological significance of contaminant levels in eggs requires knowing the comparable levels that are associated (usually experimentally) with adverse effects. Such information comes from laboratory studies (Eisler, 1985a,b, 1986, 1988). More data are available for mercury (Burger and Gochfeld, 1997) than for the other metals. Many laboratory studies give dose and effects, but do not examine tissue levels (Burger and Gochfeld, 1997, 2001). Conversely, field studies may yield tissue or egg levels without being linked to effects. Another method of evaluating effects is to compare the levels found in a target population with those normally occurring in similar species of birds, in this case several taxa of fish-eating birds, that do not seem to be adversely affected (Burger and Gochfeld, 2001). It is likely that if the levels found in eggs from a particular region are not above the median for a wide range of piscivorous species, the birds are not adversely affected. Using this method, the eggs of common terns nesting in Barnegat Bay are probably not affected by cadmium (median of 12 ngyg for fish-eating birds, and 4 ngyg for Barnegat Bay common terns, after Burger 2002). Similar comparisons are: chromium, 210 vs. 45 ngyg for Barnegat terns; and lead, 190 vs. 163 ngyg (after Burger, 2002). Remarkably few studies have examined levels of arsenic, and even the Eisler (1994) review did not report any effects studies for arsenic levels in eggs. However, the mean levels of three elements were higher in the eggs of common terns from Barnegat Bay than the median for a wide range of fish-eating birds: manganese, 510 ngyg for a range of fish-eating birds vs. 2898 ngyg for Barnegat common terns; mercury, 340 vs. 1194 ngyg; and selenium, 1100 vs. 2420 ngyg (after Burger,
2002). This suggests that these three elements bear further examination. The relationship between levels in eggs and adverse developmental effects is known for mercury (Eisler, 1987). Adverse effects, including mortality, lowered hatching rates, higher chick defects and other neurobehavioral deficits, can occur when eggs levels are as low as 500 ngyg (wet weight), and more severe effects usually occur at 1000–2000 ngyg (Eisler, 1987). Thus, the levels of mercury in eggs of common terns from Barnegat Bay appear to be within the range that might cause neurobehavioral effects. Moreover, when the egg data are examined by location, the mercury levels at Sedge Island, nearest the Little Egg Harbor Inlet, averaged 2010 ngyg. The number of common tern colonies has been declining in Barnegat Bay over the last 20 years (Burger et al., 2001). Terns that are consistently unsuccessful at raising young tend to move to other colony sites in future years. If contaminant burdens contribute to low reproductive success locally, they would be a contributing factor to regional population declines. Manganese is an essential micronutrient that is an important cofactor in metabolism (Drown et al., 1986). At high doses it is toxic. In laboratory studies, excess manganese exposure causes mortality and decreased fertility (Gray and Laskey, 1980; Laskey et al., 1982), decreases in motor activity (Ingersoll et al., 1995), learning disabilities (Senturk and Oner, 1996), and nervous system dysfunction and convulsions (Mergler, 1986). In birds, manganese causes neurobehavioral defects, similar in nature to those caused by lead (Burger and Gochfeld, 1995, 2001). Unfortunately, the levels of manganese in eggs associated with these adverse effects in chicks have not yet been determined. Selenium levels in the eggs of common terns were also above the median for other fish-eating birds (Burger, 2002), but field studies (see below) suggest that they are not at a level of concern. Selenium levels can be sufficiently high to cause adverse effects in birds (Heinz, 1996), and levels as high as 81 000 ngyg caused adverse effects in birds at Kesterson Reservoir in California (Hoffman et al., 1988). Ohlendorf et al. (1986) showed
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that adverse reproductive effects occur at approximately 10 000 ngyg of selenium in eggs, while Heinz (1996) reported that adverse reproductive effects can occur at selenium concentrations as low as 3000 ngyg (wet weight) in eggs. The levels of selenium in tern eggs from Barnegat Bay were lower (mean of 2040 ngyg). Furthermore, the levels of selenium that King et al. (1983) found in bird eggs from an uncontaminated site in Texas were similar to those of the tern eggs from Barnegat Bay. 5. Conclusions The results of this study indicate that although there are locational differences in metal levels for eggs collected from the colonies in Barnegat Bay, the differences were not great. However, mercury levels were highest nearest to an ocean inlet. Furthermore, although significant, the yearly variations were not great. The 3 years of data indicate that contaminant data from only two of these years are insufficient to determine trends, since had we used only the first 2 years we would have concluded that there were significant increases in several metals, when in fact the levels were lower in the third year. The levels of most metals do not seem sufficiently high to cause adverse effects, although the levels of mercury in eggs of some common terns from the bay are within the range known to cause adverse effects. Acknowledgments We thank R. Furness, I.C.T. Nisbet, H.M. Ohlendorf, and D. Peakall for valuable discussions about metals in seabirds; K. Cooper, M. Gallo, B.D. Goldstein and C. Powers for discussion about risk assessment; Fred Lesser for logistical help over the years; T. Shukia and C. Dixon for assistance in the laboratory; and R. Ramos for graphics. Support for the analyses was provided by the New York Bioscape Program (Wildlife Trust) and NIEHS grant ESO 5022. Research on the colonial birds in Barnegat Bay is conducted under the auspices of the Endangered and Non-Game Species Program of the New Jersey Department of Environmental Protection, and the US Environ-
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mental Protection Agency. We thank the US Fish and Wildlife Service and New Jersey Department of Environmental Protection for permits to collect specimens and conduct this research. All procedures and protocols were approved by the Rutgers University Animal Review Board. References Becker PH, Thyen S, Mickstein S, Sommer U, Schmieder KR. Monitoring pollutants in coastal bird eggs in the Wadden Sea. Wadden Sea Ecosystem No 8. Germany: Wilhelmshaven, 1998. Burger J. Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 1993;5:203 –311. Burger J. Heavy metals in avian eggshells: another excretion method. J Toxicol Environ Health 1994;41:253 –258. Burger J. Food chain differences affect heavy metals in birds in Barnegat Bay, New Jersey. Environ Res 2002;90:33 –39. Burger J, Gochfeld M. Cadmium and lead in common terns (Aves, Sterna hirundo): relationship between levels in parents and eggs. Environ Monit Assess 1991;16:253 –258. Burger J, Gochfeld M. The common tern: breeding biology and behavior. New York: Columbia University Press, 1991. Burger J, Gochfeld M. Lead and cadmium accumulation in eggs and fledgling seabirds in the New York Bight. Environ Toxicol Chem 1993;12:261 –267. Burger J, Gochfeld M. Growth and behavioral effects of early postnatal chromium and manganese exposure in herring gull (Larus argentatus) chicks. Pharmacol Biochem Behav 1995;50:607 –612. Burger J, Gochfeld M. Heavy metal and selenium levels in Franklin’s gull (Larus pipixcan) parents and their eggs. Archiv Environ Contam Toxicol 1996;30:481 –487. Burger J, Gochfeld M. Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. Environ Res 1997;75:160 –172. Burger J, Gochfeld M. Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health B 2000;3:59 –78. Burger J, Gochfeld M. Effects of chemicals and pollution on seabirds. In: Schreiber EA, Burger J, editors. Biology of marine birds. Boca Raton, FL: CRC Press, 2001. p. 485 – 525. Burger J, Jenkins CD, Lesser F, Gochfeld M. Population trends of colonially nesting birds in Barnegat Bay. J Coastal Res 2001;32:197 –211. Special issue. Drown DB, Oberg SG, Sharma RP. Pulmonary clearance of soluble and insoluble forms of manganese. J Toxicol Environ Health 1986;17:201 –212. Eisler R. Selenium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service Biology Report 85 (噛1.5) 1985. Eisler R. Cadmium hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service Biology Report 85 (噛1.2). 1985.
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