METALS
IN TERN
EGGS
IN A NEW JERSEY
ESTUARY:
A D E C A D E OF C H A N G E JOANNA
BURGER
and M I C H A E L
GOCHFELD
.Department o f Biological Sciences and Environmental and Occupational Health Sciences Institute, Rutgers University, Piscataway, N J 08855, U.S.A. and
Department o f Environmental & Community Medicine and Environmental and Occupational Health Sciences Institute, UMDNJ-Robert Wood Johnson Medical School, Piscataway, N J 08854, U.S.A.
(Received 4 March, 1988; accepted September, 1988) Abstract. We compared levels of eight heavy metals in c o m m o n tern eggs collected in 1982 (n = 24) from coastal New Jersey with archived specimens collected from the same colonies in 1971 ( N = 9 ) . Levels o f all metals, except cobalt, showed a significant decrease over the 11 year period, with lead and nickel showing the greatest decline. Mercury levels declined over 50~ based on geometric means. C a d m i u m and mercury showed the lowest levels in both years. Pair-wise correlation coefficients on log-transformed data revealed lower correlations in 1971, whereas most metal pairs showed significant correlations in 1982. Mercury levels showed significant positive correlations with cobalt, cadmium, and nickel in 1971, but were not correlated with levels o f any other metal in 1982.
I. Introduction
Pollutants enter the food chain through the biota and through air and water. Heavy metals are derived from industrial effluents, agricultural runoff, and air pollution fallout, as well as natural erosion and biogeochemical cycles. Once a metal has entered the body it may be stored in the tissues or excreted. Numerous studies have examined the bioaccumulation or tissue levels of pollutants in such diverse groups as birds (Maedgen et al., 1982; Howarth et al., 1982) mammals (Mobarak and P'an, 1984; Wren, 1986), fish (Rohrer et al., 1982; DeVault, 1985), and invertebrates (Harrison et al., 1984; Honda et al., 1984; Elliott et al., 1986). Fimreite et al., (1974, 1982) noted that female birds eliminate pollutants such as organochlorines and some heavy metals by sequestering them in their eggs, a phenomenon which may jeopardize the developing embryos (Romanoff and Romanoff, 1972). Some experimentally dosed female birds with elevated tissue levels have failed to show detectable levels of heavy metals in their eggs (Eastin and O'Shea, 1981; Pattee, 1984). Nonetheless, several studies of avian eggs from nature have shown elevated levels of mercury (Fimreite et al., 1974, 1982; Haseltine et al., 1980, 1981), lead and cadmium (Maedgen et al., 1982), and other metals (Gochfeld and Burger, 1987), indicating that females do sequester certain metals in their eggs under certain conditions. Several authors have reported residues of organochlorines (Haseltine et al., 1981; Blus and Lamont, 1979; Lemmetyinen et aL, 1982; Ohlendorf et al., 1982, 1985; Custer et al., 1983) and heavy metals in eggs of a variety of bird species. Frequently Environmental Monitoring and Assessment 11: 127-135, 1988. 9 1988 Kluwer Academic Publishers. Printed in the Netherlands.
128
JOANNA
BURGER
AND
MICHAEL
GOCHFELD
these studies have reported levels o f organochlorines and perhaps a single metal (e.g., mercury, Peterson and Ellarson, 1976; Weseloh et al., 1983; Haseltine et al., 1983). Several studies have examined heavy metal levels comparing a variety of avian species (Fimreite et al., 1974), in different locations (Haseltine et al., 1980; Peterson and Ellarson, 1976; Blus et al., 1985), or different colonies (Blus et al., 1974) over a one or two year period. Connors et al. (1975) reported levels of eight metals in several tissues o f common terns (Sterna hirundo) from several colonies scattered through two geographic regions, for a single year. There are few longer-term studies on either organochlorines or heavy metals, although Fimreite et al. (1982) examined organochlorines and mercury over an eight year period in Northern gannets (Morrus bassanus). Blus and Lamont (1979) examined organochlorine levels in eggs of six estuarine bird species over a five year period. With an increase in environmental consciousness and stricter regulations in the 1970's, it appeared likely that the levels of several pollutants would have declined. For example, the great decrease in leaded gasoline is a major contributor to reduced lead levels in the environment and in humans (C.D.C., 1982). Such decreases should be reflected in lower levels of metals in adult tissues and eggs o f birds. In this paper we analyze data on heavy metal levels in eggs of common terns (Sterna hirundo) from the coast o f New Jersey, comparing 1971 and 1982. The common tern is a highly migratory species, and would not be the first choice if one were interested in monitoring a specific local pollution phenomenon. However, because of an epidemic o f developmental defects which afflicted breeding colonies o f this species (Hays and Risebrough, 1972; Gochfeld, 1975) throughout the New York Bight, we had previously archived a small sample o f c o m m o n tern eggs from 1971, and this archive forms the basis for the present study. We test the following null hypotheses: (1) There are no temporal differences in metal levels in tern eggs, (2) There are no temporal differences in the relationships (or correlation patterns) among different metals. In Long Island and New Jersey, the area referred to as the New York Bight, c o m m o n terns breed in colonies ranging from several to thousands of pairs, on vegetated sandy beaches, and salt marshes, on estuarine and offshore islands (Gochfeld, 1976; Burger and Lesser, 1978). They migrate over the oceans and overwinter along the coasts of South America. The terns are piscivorous, feeding high on the food chain, and thus may be exposed to biologically amplified levels of metals. Heavy metal levels in breeding adults and eggs have been reported from both Lake Ontario and Long Island (Gochfeld and Burger, 1987; Connors et al., 1975). 2. Materials and Methods
Under appropriate federal and state permits we collected eggs from common tern breeding colonies in 1971 ( n = 9 ) and 1982 ( n = 2 4 ) within 3-4 days of laying. Eggs were collected from Ham, Pettit and Vol Sedge Islands in Barnegat Bay. All eggs were collected in late May at the beginning of the egg-laying period. In both years
129
M E T A L S IN T E R N E G G S IN A N E W J E R S E Y E S T U A R Y : A D E C A D E O F C H A N G E
we t o o k o n l y o n e egg f r o m a n y nest. I n the l a b o r a t o r y the freshly-collected eggs were weighed, m e a s u r e d a n d dissected. T h e entire c o n t e n t s o f the egg were weighed i m m e d i a t e l y , a n d this flesh wet weight was the basis for all reported c o n c e n t r a t i o n s . Samples were frozen in triple-rinsed (deionized water) plastic c o n t a i n e r s . All samples f r o m 1971 a n d 1982 were a n a l y z e d at the same time. P r e p a r a t i o n , e x t r a c t i o n a n d analytic procedures followed the E n v i r o n m e n t a l P r o t e c t i o n A g e n c y p r o t o c o l for tissues ( E . P . A . , 1980). Tissues were digested in w a r m nitric-sulfuric acid m i x t u r e with the a d d i t i o n o f 50O7o h y d r o g e n peroxide a n d were s u b s e q u e n t l y diluted in deionized water. M e r c u r y was a n a l y z e d b y cold v a p o r t e c h n i q u e , the other metals b y graphite f u r n a c e a t o m i c a b s o r p t i o n . All c o n c e n t r a t i o n s are expressed in ng g - 1 (parts per billion) o n a fresh wet weight basis using weights o b t a i n e d at the time the specimens were collected. D e t e c t i o n limits for the metals r a n g e d f r o m 0.3 p p b to a b o u t 10 ppb. All specimens were r u n in batches with spiked specimens, a n d the recovery percentage r a n g e d f r o m 78-92o/o. T h e coefficient o f v a r i a t i o n o n replicate spiked samples r a n g e d f r o m 6-21 o7o. F u r t h e r q u a l i t y c o n t r o l include periodic b l i n d analysis o f a n a l i q u o t f r o m a large sample o f k n o w n metal c o n c e n t r a t i o n . W e used S.A.S. n o n - p a r a m e t r i c procedures to c o m p a r e levels a m o n g years ( S . A . S . , 1982). P e a r s o n P r o d u c t - m o m e n t c o r r e l a t i o n coefficients were c o m p u t e d o n l o g - t r a n s f o r m e d data.
3. R e s u l t s
3.1. INTERYEAR COMPARISON Except for cobalt, c o n c e n t r a t i o n s o f all 8 metals were significantly lower in 1982 t h a n in 1971 (Table I). I n b o t h years nickel a n d zinc showed the highest c o n c e n t r a t i o n s ,
TABLE I Comparison of metal levels in common tern eggs in 1971 and 1982. Levels in ppb (ng g- ~based on fresh wet weight) Arithmetic Means 1971 Number Cadmium Cobalt Copper Lead Mercury Manganese Nickel Zinc a
9 455 + 74 741_ 282 3790 + 406 2 880- 853 648 + 72 2680 + 524 5190 + 412 43200_.+3 170
Geometric Means 1982 24 156+ 20 537+ 38 913 + 127 446 + 81 337 + 82 578+ 108 1050__. 205 22000__.4320
X 2(p)a
5.7 (.02) 0.2 (NS) 14.6 (.0001) 7.0 (.008) 8.7 (.003) 12.3 (,0005) 13.3(,0005) 10.6 (.001)
Kruskal-Wallis chi square from S.A.S. PROC NPARIWAY.
1971
1982
Ratio
388 478 3610 1980 614 2290 6380 42300
147 498 882 428 253 480 1070 17500
2.6 0.9 4.1 4.6 2.4 4.7 6.0 2.4
130
JOANNA BURGER AND MICHAEL GOCHFELD
while c a d m i u m a n d m e r c u r y were lowest. Metal c o n c e n t r a t i o n s were a b o u t 2 to 6 fold lower in 1982 c o m p a r e d to 1971. E v e n the c o n c e n t r a t i o n s o f cobalt, m e r c u r y , a n d zinc declined b y m o r e t h a n 50O7o f r o m 1971 to 1982. 3.2. INDIVIDUAL PATTERN COMPARISONS R e p o r t i n g m e a n values for metal levels in eggs for colonies or years partly obscures i n d i v i d u a l patterns. Some individuals m a y show high levels for all metals; alternatively there m a y be n o c o r r e l a t i o n a m o n g certain metals. W e c o m p a r e d c o r r e l a t i o n coefficients a m o n g metals for 1971 a n d for 1982. F o r 1971 most metal pairs were n o t significantly correlated. Eggs t h a t were high in o n e metal were n o t necessarily high for other metals. I n 1971 the o n l y positive correlations ( P < 0.05) were for m e r c u r y with c a d m i u m , cobalt, a n d nickel; c a d m i u m with cobalt; a n d copper with zinc (upper right h a n d p o r t i o n o f T a b l e I). H o w e v e r , there was a strong t e n d e n c y for significant positive c o r r e l a t i o n s in the 1982 sample (lower left h a n d p o r t i o n o f T a b l e II). Surprisingly in 1982 m e r c u r y showed n o significant correlations with other metals.
T A B L E II C o r r e l a t i o n c o e f f i c i e n t s f o r m e t a l levels in c o m m o n t e r n eggs f o r 1971 ( a b o v e d i a g o n a l , N = 9 ) ( b e l o w d i a g o n a l , M = 24) *
IN TERN
EGGS
IN A NEW JERSEY
ESTUARY:
A D E C A D E OF C H A N G E JOANNA
BURGER
and M I C H A E L
GOCHFELD
.Department o f Biological Sciences and Environmental and Occupational Health Sciences Institute, Rutgers University, Piscataway, N J 08855, U.S.A. and
Department o f Environmental & Community Medicine and Environmental and Occupational Health Sciences Institute, UMDNJ-Robert Wood Johnson Medical School, Piscataway, N J 08854, U.S.A.
(Received 4 March, 1988; accepted September, 1988) Abstract. We compared levels of eight heavy metals in c o m m o n tern eggs collected in 1982 (n = 24) from coastal New Jersey with archived specimens collected from the same colonies in 1971 ( N = 9 ) . Levels o f all metals, except cobalt, showed a significant decrease over the 11 year period, with lead and nickel showing the greatest decline. Mercury levels declined over 50~ based on geometric means. C a d m i u m and mercury showed the lowest levels in both years. Pair-wise correlation coefficients on log-transformed data revealed lower correlations in 1971, whereas most metal pairs showed significant correlations in 1982. Mercury levels showed significant positive correlations with cobalt, cadmium, and nickel in 1971, but were not correlated with levels o f any other metal in 1982.
I. Introduction
Pollutants enter the food chain through the biota and through air and water. Heavy metals are derived from industrial effluents, agricultural runoff, and air pollution fallout, as well as natural erosion and biogeochemical cycles. Once a metal has entered the body it may be stored in the tissues or excreted. Numerous studies have examined the bioaccumulation or tissue levels of pollutants in such diverse groups as birds (Maedgen et al., 1982; Howarth et al., 1982) mammals (Mobarak and P'an, 1984; Wren, 1986), fish (Rohrer et al., 1982; DeVault, 1985), and invertebrates (Harrison et al., 1984; Honda et al., 1984; Elliott et al., 1986). Fimreite et al., (1974, 1982) noted that female birds eliminate pollutants such as organochlorines and some heavy metals by sequestering them in their eggs, a phenomenon which may jeopardize the developing embryos (Romanoff and Romanoff, 1972). Some experimentally dosed female birds with elevated tissue levels have failed to show detectable levels of heavy metals in their eggs (Eastin and O'Shea, 1981; Pattee, 1984). Nonetheless, several studies of avian eggs from nature have shown elevated levels of mercury (Fimreite et al., 1974, 1982; Haseltine et al., 1980, 1981), lead and cadmium (Maedgen et al., 1982), and other metals (Gochfeld and Burger, 1987), indicating that females do sequester certain metals in their eggs under certain conditions. Several authors have reported residues of organochlorines (Haseltine et al., 1981; Blus and Lamont, 1979; Lemmetyinen et aL, 1982; Ohlendorf et al., 1982, 1985; Custer et al., 1983) and heavy metals in eggs of a variety of bird species. Frequently Environmental Monitoring and Assessment 11: 127-135, 1988. 9 1988 Kluwer Academic Publishers. Printed in the Netherlands.
128
JOANNA
BURGER
AND
MICHAEL
GOCHFELD
these studies have reported levels o f organochlorines and perhaps a single metal (e.g., mercury, Peterson and Ellarson, 1976; Weseloh et al., 1983; Haseltine et al., 1983). Several studies have examined heavy metal levels comparing a variety of avian species (Fimreite et al., 1974), in different locations (Haseltine et al., 1980; Peterson and Ellarson, 1976; Blus et al., 1985), or different colonies (Blus et al., 1974) over a one or two year period. Connors et al. (1975) reported levels of eight metals in several tissues o f common terns (Sterna hirundo) from several colonies scattered through two geographic regions, for a single year. There are few longer-term studies on either organochlorines or heavy metals, although Fimreite et al. (1982) examined organochlorines and mercury over an eight year period in Northern gannets (Morrus bassanus). Blus and Lamont (1979) examined organochlorine levels in eggs of six estuarine bird species over a five year period. With an increase in environmental consciousness and stricter regulations in the 1970's, it appeared likely that the levels of several pollutants would have declined. For example, the great decrease in leaded gasoline is a major contributor to reduced lead levels in the environment and in humans (C.D.C., 1982). Such decreases should be reflected in lower levels of metals in adult tissues and eggs o f birds. In this paper we analyze data on heavy metal levels in eggs of common terns (Sterna hirundo) from the coast o f New Jersey, comparing 1971 and 1982. The common tern is a highly migratory species, and would not be the first choice if one were interested in monitoring a specific local pollution phenomenon. However, because of an epidemic o f developmental defects which afflicted breeding colonies o f this species (Hays and Risebrough, 1972; Gochfeld, 1975) throughout the New York Bight, we had previously archived a small sample o f c o m m o n tern eggs from 1971, and this archive forms the basis for the present study. We test the following null hypotheses: (1) There are no temporal differences in metal levels in tern eggs, (2) There are no temporal differences in the relationships (or correlation patterns) among different metals. In Long Island and New Jersey, the area referred to as the New York Bight, c o m m o n terns breed in colonies ranging from several to thousands of pairs, on vegetated sandy beaches, and salt marshes, on estuarine and offshore islands (Gochfeld, 1976; Burger and Lesser, 1978). They migrate over the oceans and overwinter along the coasts of South America. The terns are piscivorous, feeding high on the food chain, and thus may be exposed to biologically amplified levels of metals. Heavy metal levels in breeding adults and eggs have been reported from both Lake Ontario and Long Island (Gochfeld and Burger, 1987; Connors et al., 1975). 2. Materials and Methods
Under appropriate federal and state permits we collected eggs from common tern breeding colonies in 1971 ( n = 9 ) and 1982 ( n = 2 4 ) within 3-4 days of laying. Eggs were collected from Ham, Pettit and Vol Sedge Islands in Barnegat Bay. All eggs were collected in late May at the beginning of the egg-laying period. In both years
129
M E T A L S IN T E R N E G G S IN A N E W J E R S E Y E S T U A R Y : A D E C A D E O F C H A N G E
we t o o k o n l y o n e egg f r o m a n y nest. I n the l a b o r a t o r y the freshly-collected eggs were weighed, m e a s u r e d a n d dissected. T h e entire c o n t e n t s o f the egg were weighed i m m e d i a t e l y , a n d this flesh wet weight was the basis for all reported c o n c e n t r a t i o n s . Samples were frozen in triple-rinsed (deionized water) plastic c o n t a i n e r s . All samples f r o m 1971 a n d 1982 were a n a l y z e d at the same time. P r e p a r a t i o n , e x t r a c t i o n a n d analytic procedures followed the E n v i r o n m e n t a l P r o t e c t i o n A g e n c y p r o t o c o l for tissues ( E . P . A . , 1980). Tissues were digested in w a r m nitric-sulfuric acid m i x t u r e with the a d d i t i o n o f 50O7o h y d r o g e n peroxide a n d were s u b s e q u e n t l y diluted in deionized water. M e r c u r y was a n a l y z e d b y cold v a p o r t e c h n i q u e , the other metals b y graphite f u r n a c e a t o m i c a b s o r p t i o n . All c o n c e n t r a t i o n s are expressed in ng g - 1 (parts per billion) o n a fresh wet weight basis using weights o b t a i n e d at the time the specimens were collected. D e t e c t i o n limits for the metals r a n g e d f r o m 0.3 p p b to a b o u t 10 ppb. All specimens were r u n in batches with spiked specimens, a n d the recovery percentage r a n g e d f r o m 78-92o/o. T h e coefficient o f v a r i a t i o n o n replicate spiked samples r a n g e d f r o m 6-21 o7o. F u r t h e r q u a l i t y c o n t r o l include periodic b l i n d analysis o f a n a l i q u o t f r o m a large sample o f k n o w n metal c o n c e n t r a t i o n . W e used S.A.S. n o n - p a r a m e t r i c procedures to c o m p a r e levels a m o n g years ( S . A . S . , 1982). P e a r s o n P r o d u c t - m o m e n t c o r r e l a t i o n coefficients were c o m p u t e d o n l o g - t r a n s f o r m e d data.
3. R e s u l t s
3.1. INTERYEAR COMPARISON Except for cobalt, c o n c e n t r a t i o n s o f all 8 metals were significantly lower in 1982 t h a n in 1971 (Table I). I n b o t h years nickel a n d zinc showed the highest c o n c e n t r a t i o n s ,
TABLE I Comparison of metal levels in common tern eggs in 1971 and 1982. Levels in ppb (ng g- ~based on fresh wet weight) Arithmetic Means 1971 Number Cadmium Cobalt Copper Lead Mercury Manganese Nickel Zinc a
9 455 + 74 741_ 282 3790 + 406 2 880- 853 648 + 72 2680 + 524 5190 + 412 43200_.+3 170
Geometric Means 1982 24 156+ 20 537+ 38 913 + 127 446 + 81 337 + 82 578+ 108 1050__. 205 22000__.4320
X 2(p)a
5.7 (.02) 0.2 (NS) 14.6 (.0001) 7.0 (.008) 8.7 (.003) 12.3 (,0005) 13.3(,0005) 10.6 (.001)
Kruskal-Wallis chi square from S.A.S. PROC NPARIWAY.
1971
1982
Ratio
388 478 3610 1980 614 2290 6380 42300
147 498 882 428 253 480 1070 17500
2.6 0.9 4.1 4.6 2.4 4.7 6.0 2.4
130
JOANNA BURGER AND MICHAEL GOCHFELD
while c a d m i u m a n d m e r c u r y were lowest. Metal c o n c e n t r a t i o n s were a b o u t 2 to 6 fold lower in 1982 c o m p a r e d to 1971. E v e n the c o n c e n t r a t i o n s o f cobalt, m e r c u r y , a n d zinc declined b y m o r e t h a n 50O7o f r o m 1971 to 1982. 3.2. INDIVIDUAL PATTERN COMPARISONS R e p o r t i n g m e a n values for metal levels in eggs for colonies or years partly obscures i n d i v i d u a l patterns. Some individuals m a y show high levels for all metals; alternatively there m a y be n o c o r r e l a t i o n a m o n g certain metals. W e c o m p a r e d c o r r e l a t i o n coefficients a m o n g metals for 1971 a n d for 1982. F o r 1971 most metal pairs were n o t significantly correlated. Eggs t h a t were high in o n e metal were n o t necessarily high for other metals. I n 1971 the o n l y positive correlations ( P < 0.05) were for m e r c u r y with c a d m i u m , cobalt, a n d nickel; c a d m i u m with cobalt; a n d copper with zinc (upper right h a n d p o r t i o n o f T a b l e I). H o w e v e r , there was a strong t e n d e n c y for significant positive c o r r e l a t i o n s in the 1982 sample (lower left h a n d p o r t i o n o f T a b l e II). Surprisingly in 1982 m e r c u r y showed n o significant correlations with other metals.
T A B L E II C o r r e l a t i o n c o e f f i c i e n t s f o r m e t a l levels in c o m m o n t e r n eggs f o r 1971 ( a b o v e d i a g o n a l , N = 9 ) ( b e l o w d i a g o n a l , M = 24) *
