Estuaries Vol. 14, No. 3, p. 299-305 September 1991

Multidisciplinary Assessment of Pollution

in Long Island Sound

at Three Sites

WILLIAM D. GRONLUND JOHN E. STEIN

SIN-LAM CHAN DONALD W . BROWN

BRUCE B. MCCAIN J O H N T . LANDAHL

ROBERT C. CLARK, JR. MARGARET M. KRAHN

MARK S. MYERS USHA VARANASI

Environmental Conservation Division Northwest Fisheries Center National Marine Fisheries Service National Oceanic and Atmospheric Administration 2725 Montlake Boulevard East Seattle, Washington 98112

ABSTRACT: Winter f lounder (Pseudopleuronectes americanus) were sampled f rom three sites located near Nor- walk, New Haven, and Niantic, Connecticut, in Long Is land Sound du r ing February 1987, to evaluate the degree of chemical con tamina t ion and to de termine possible effects of con taminant exposure. At each site, sediment and in fauna l inver tebrates were also collected and analyzed for trace metals and organic chemicals. Specimens of l iver and kidney f rom winter f lounder were examined for histopathological condit ions, inc luding the presence of mac- rophage aggregates in l iver tissue. Liver samples were also analyzed for DNA damage (i.e., the format ion of adducts between DNA and chemical contaminants) . Blood samples were collected and analyzed for erythrocyte micronuclei . The sampl ing site near New Haven was de termined to be the most affected site, f rom the s tandpoints of greater chemical con tamina t ion and possible effects on winter flounder. Concentra t ions of aromatic hydrocarbons (AHs) and polychlor inated biphenyls (PCBs) were highest in sediment f rom this site, and the highest prevalences of the histopathological changes and DNA al terat ions were also found in the l ivers of winter f lounder f rom this site. No differences in the concentra t ions of contaminants in fish or in frequencies of erythrocyte micronuclei in fish blood were found between sites. None of the sites sampled had con taminan t levels or prevalences of lesions as h igh as previously found at o ther East Coast locations (e.g., Boston Harbor , Massachusetts, Rar i tan Bay, New York). Overall , our results indicate moderate levels of pol lut ion at two of the u rban sites in Long Is land Sound and provide a f ramework for expanded studies to bet ter define the extent and impact of chemical pol lut ion in Long Is land Sound.

Int roduct ion

Long Island Sound, located within the states of New York and Connecticut, is a major shipping route and is heavily used seasonally for pleasure boating. In addition, the area supports a large rec- reational fishery (Poole 1966; Mohr 1976). Earlier reports on contaminant concentrations and asso- ciated effects in Long Island Sound (Greig et al. 1977; Hunt 1979; Reid 1983) emphasized primar- ily trace metal contamination and effects inferred from laboratory bioassays. More recent reports (Zdanowicz et al. 1986; Turgeon and O'Connor 1991) have included more information on organic chemical contaminants in sediments and biota and potential effects on fish. In this paper we present results of analyses of a broad range of organic and inorganic chemical contaminants in sediments, se- lected infaunal invertebrates, and tissue and stom- ach contents of winter flounder (Pseudopleuronectes americanus) and of measurements of biological ef-

fects in winter flounder sampled from three sites in Long Island Sound.

Sediments serve as a repository for a large num- ber of environmental contaminants, particularly those that are relatively water insoluble (Malins et al. 1984; O'Conner and Huggett 1988). Fish can accumulate chemical contaminants from multiple sources, including sediments (Eadie et al. 1982; Gossett et al. 1983; Varanasi et al. 1985). The pres- ence of selected chemical contaminants, along with certain histopathological conditions in fish liver, such as neoplasms and macrophage aggregates, serve as useful indicators of environmental deg- radation (Murchelano and Wolke 1985; Wolke et al. 1985; Blazer et al. 1987; Myers et al. 1987).

In addition to histopathology, other approaches have been suggested as indicators of possible ef- fects of environmental degradation by toxic chem- icals: measurement of DNA damage (adducts) in marine fish (Varanasi et al. 1989b, c), and the quan-

�9 1991 Estuarine Research Federation 299 0160-8347/91/030299-07501.50/0

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Fig. 1. Location of sampling sites in Long Island Sound�9

titation of micronuclei in fish erythrocytes (Hose et al. 1987).

Accordingly, in this study, we have measured all these parameters to evaluate their significance in assessing levels and impact of contamination.

Methods

Samples were collected aboard the NOAA ship Ferrel in February 1987 at three sites in Long Is- land Sound (Fig. 1). The sites, which were thought to represent a range of chemical contamination, from west to east were located at the mouth of the Norwalk River, near Norwalk, Connecticut; at Morris Cove, south of New Haven, Connecticut; and at Niantic Bay, south of Niantic, Connecticut. Additional samples of winter flounder were col- lected from the Niantic site in winter 1988 and spring 1989. Similarly collected samples were ob- tained from a site near Deer Island in Boston Har- bor in winter 1988 and some results were included here for comparative purposes.

Fish were collected with otter trawl and sediment was collected with either a 0.1 m ~ box corer or a modified Van Veen grab. At each site the first 30 adult fish collected were dissected. Three sets of three sediment grabs were used at each fishing site for collection of sediment for chemical analysis�9 Procedures for collecting sediments and winter flounder for analytical chemistry and for histo- pathological evaluations followed protocols devel- oped for the National Benthic Surveillance Project (NBSP) of NOAA's National Status and Trends Program (Krahn et al. 1988; Varanasi et al. 1989a).

Bile florescent aromatic compounds (FACs) were determined by high pressure liquid chromatogra- phy (Krahn et al. 1986). Otoliths were examined to determine the age of each fish. Assessment of liver macrophage aggregates was done by estimat- ing cellular density and calculating a relative index (Wolke et al. 1985). The levels of DNA-xenobiotic adducts in liver were assessed using s~p labelling and autoradiography (Varanasi et al.. 1989c). In- vertebrates seived from sediment were used for organic chemical analysis.

Sheffes F-test (Zar 1984) was used to compare differences in mean levels of DNA adducts in win- t er flounder livers. Fisher's Exact test (Zar 1984) was used to test for significance of differences in prevalences of lesions in tissue specimens of winter flounder. The relative macrophage aggregate in- dices of the liver of individual winter flounder were compared with the Kruskal-Wallis test (Zar 1984). Comparison intervals were calculated for graphical comparisons of significant differences in levels of organic chemicals and trace metals in sediments and liver (Gabriel 1978; Sokal and Rohlf 1981). When examining comparison intervals, overlap- ping intervals indicate means that are not signifi- cantly different. For all statistical analyses per- formed, probabilities less than or equal to 0.05 were considered significant�9

Results

The evidence suggests that winter flounder from the New Haven site showed the greatest changes in certain biochemical and pathological character-

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120.

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[] pronfel ve �9 :~::~ii~ili::~iii:~ii:ii,::i:.i,~ i~i :: [] SDN ::ii~: ~i: a !ii~: i ~:~::~: i [] pre-neoplasms .:...:.:...:.:.:...:.:...:.:.:.. i~! :~i!ii~i:~:i::~i~:i~:i:~ii~:!i:i:: �9 neoplasms

:::::::::::::::::::::::::::::: 2

29 20 lao

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New Haven Norwalk Niantic 87 Niantic 87-89

Fig. 2. Cumulative prevalence (%) of eight categories of histopathological lesions in liver of winter flounder from New Haven, Norwalk, and Niantic Bay. Numbers above bars denote sample size. Lower case letters indicate results of statistical test- ing.

istics and fish from the Niantic site had the least. The New Haven site generally had the highest lev- els of organic chemical contamination of sediment of the three sites sampled in Long Island Sound, whereas the site at Niantic had the lowest levels. The following sections describe the results on bi- ological effects and the results of chemical analysis of sediment and tissue.

BIOLOGICAL EFFECTS

Histopathological Conditions in Liver and Kidney

The highest prevalences of liver abnormalities were found in winter flounder collected at the New IIaven and Norwalk sites (Fig. 2). In 1987, New Haven was the only site where hepatic neoplasms were detected (3.3%, n = 30). The additional data from fish collected during 1988-1989 at Niantic confirms the low frequencies of liver pathology in fish from this site.

The difference in the prevalence of specific de- generative necrosis (SDN) in the livers of fish col- lected in 1987 is especially notable [10% at New Haven compared to 0% at Niantic (n = 29)], be- cause this type of lesion in other fish species is significantly correlated with exposure to chemical

Pollution Assessment in Long Island Sound 301

Niantic 87-89 t

Niantic 87 1

Norwalk 1

New Haven 1

Boston 88 1

0

a = significantly different (P<0.05) from Nianfic 87 by Kruska]-Wallis test

�9 132

�9 29

�9 29a

� 9

�9 51

relative concentration of maerophage aggregates

Fig. 3. Relative concentration of macrophage aggregates in liver of winter flounder from Niantic, Norwalk, New Haven, and Boston Harbor. Numbers indicate sample size and lower case letters denote results of statistical testing.

contaminants (Malins et al. 1984) and is interpret- ed to be the result of chronic exposure to toxic agents (Myers et al. 1987).

Similarly, the prevalence of severe hydropic de- generation (SHD) in the hepatic parenchyma of winter flounder from the Niantic site was signifi- cantly lower than the prevalences of this condition at the other sites (Fig. 2). This lesion type has been reported to co-occur with degenerative, neoplastic, and other proliferative lesions in winter flounder from polluted sites such as Boston Harbor (Mur- chelano and Wolke 1985), and appears to be in- dicative of an increased rate of cell death and turn- over of hepatocytes and biliary epithelial cells, probably as a result of exposure to toxic agents.

The liver macrophage aggregate (MA) index was consistently and significantly lower for all age groups of winter flounder examined at the Niantic site in 1987 (Fig. 3). In succeeding years, additional samples from the Niantic site confirmed the low frequency of this condition. The MA index in fish from the New Haven site was nearly identical with that for fish sampled at the site near Deer Island in Boston Harbor in 1988. The presence of liver MA in winter flounder from nonurban sites, even though the index values are low, suggests that this condition is not strictly a pathological change, but rather a normal feature of winter flounder liver. It appears, therefore, that high liver MA index values are a response to exposure to "stressful" environmental stimuli including chemical contam- ination (Wolke et al. 1985).

Although many pathological conditions do have a tendency to increase in frequency in older fish, age differences between sites did not appear to be a factor in the differences in prevalences, because the average age of fish (4 yr) at each site was nearly identical.

Potentially contaminant-associated lesions in the kidney (necrosis or mesangiolysis) were found only in fish from the New Haven site, at a prevalence of 3%. No other pathological conditions of the kidney were detected in any of the fish examined.

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Levels of Hepatic DNA Adducts

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T T Boston New Norwalk Niantic Harbor Haven (reference)

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Fig. 4. Levels of hepatic DNA adducts in winter flounder from three sites in Long Island Sound and a contaminated site in Boston Harbor. (Circles indicate means, n denotes sample size, and vertical bars indicate standard deviation.)

DNA Adducts The levels of hepatic DNA-xenobiotic adducts

in winter f lounder f rom the New Haven site were significantly higher than the levels in f lounder from the o ther sites. T h e level of adducts in fish from the Norwalk site was similar to those in fish from the Niantic site (Fig. 4). As was found with hepatic MA, the levels of hepatic DNA-xenobiotic adducts in fish from the New Haven site were almost iden- tical to those found in winter f lounder from the contaminated site in Boston Harbor .

Erythrocyte Micronuclear Abnormalities No differences were found among the sites in

frequencies of erythrocyte micronuclei or o ther nuclear characteristics in the blood of winter floun- der. These observations agree with those of Car- rasco et al. (1990) for o ther species off ish exposed to chemical contamination.

CHEMICAL C O N T A M I N A T I O N

Aromatic Hydrocarbons (AHs) Sediment concentrat ions of AHs were signifi-

cantly different among all sites, with the highest mean concentrat ion in sediments f rom the New Haven site and the lowest mean concentrat ion in samples f rom the Niantic site (Fig. 5). T h e con- centrations of AHs in infaunal invertebrates (poly- chaetes) and fish stomach contents (various pro- portions ofpolychaetes , molluscs, and crustaceans) were also highest at the New Haven site. However, these analyses were done on pooled samples which

New Haven sediment

invertebrates

stomach contents

N0rwalk sediment

invertebrates

stomach contents

Niantic sediment

invertebrates

stomach contents

Aromatic Hydrocarbons

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a

a

a = significantly different P_<0.05 from all other sites by comparison intervals

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Fig. 5. Concentrat ions (ng g-l dry wt) of aromatic hydro- carbons (AHs) in sediment, infaunal invertebrates, and stomach contents of winter flounder. Clear squares indicate means + comparison intervals. Solid square indicates results of analysis of composites. Lower case letters denote results of statistical testing.

precluded statistical analysis of differences be- tween sites. These concentrat ions were consider- ably lower than the sediment concentrations of AHs at each site, suggesting that infaunal invertebrates were not bioconcentrat ing AHs.

Since aromatic hydrocarbons are rapidly metab- olized in fish (Varanasi et al. 1985) and are gen- erally at levels below detection limits in liver tissue, analysis of bile for florescent aromatic compounds was used (Krahn et al. 1986) as an indicator of recent exposure to aromatic hydrocarbon com- pounds. These measurements had high variability (Fig. 6), and no significant differences between sites were observed. The apparent anomaly indicated

Bile FACs

Niantie

Norwalk

New Haven

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Nianfie ~ FAC BaP

Norwalk

New Haven - - ~

o 3~o ~ ~o llOO l~o llOO FACs (ng eqivalents / g bile)

Fig. 6. Average concentrat ions (+ standard deviation) of fluorescent aromatic compounds determined at naphthalene wavelengths (FACs NPH) and at benzo[a]pyrene wavelengths (FACs BaP) in bile of winter flounder.

Niantic sediment

invertebrates

stomach contents

liver

Norwalk sediment

invenebrdtes

stomach Contents

liver

New Haven sediment

invertebrates

stomach contents

liver

0

PCB

64 ng g-I

145 ng g-I

I I

a = significantly different P<0.05 from Norwalk and Niantie by

246 ng g-I a comparison intervals

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a~bo 60bo 9~0 12~0 1.~0 ng g-I dry weight

Fig. 7. Concentrations (ng g t dry wt) of PCBs in sediment, infaunal invertebrates, and stomach contents and liver of winter flounder. Open squares indicate means • comparison intervals. Solid squares indicate results of analysis of composites. The numbers associated with the mean sediment concentrations are the actual levels. Lower case letters denote results of statistical analysis.

by the low levels o f FACs in bile o f fish f rom N e w Haven ( compared to sed iment concentrat ions o f AHs) may have been related to the late spawning stage o f fish f rom this site c o m p a r e d to the fish f rom the o ther sites.

Chlorinated Hydrocarbons T h e m e a n concentra t ion o f po lychlor inated bi-

phenyls (PCBs) in sed iment was significantly h igher

Nianfic Norwalk

New Haven

Nianfic Norwalk

New Haven

Niantic Norwalk

New Haven

Niantic Norwalk

New Haven

Niantie Norwalk

New Haven

Niamie Norwalk

New Haven

Fig. 8.

Tin b --significantly different P_<0.05 from Niantie by c o m p ~ inteawals

~ ' ~ b Nickel

�9 , b L e a d : -- : b

c = significantly different P_<0.05 from New Haven by comparison intervals

, b Copper ue Jb

I i I : : b Chromium I = tb

I �9 i b Z i n c

0 100 200 300 p.g gq dry weight

Concentrations (~g g-~ dry wt) of zinc, chromium, copper, lead, nickel, and tin in sediments from New Haven, Norwalk, and Niantic. Squares represent means • comparison intervals. Lower case letters indicate results of statistical testing.

Pollution A s s e s s m e n t in Long Is land S o u n d 303

Niantic

Norwalk

New Haven

Niantie

Norwalk

New Haven

Niantic Norwalk

New Haven

Silver

ill b Antimony

~ b

a = significantly different P~-0.05 from Niantic and Norwalk by comparison intervals

b = significantly different P:S'0.05 from Nianfir by comparison intervals

i N b Mercury

~ b

p.g gq dry weight

Fig. 9. Concentrations (#g g-~ dry wt) of silver, antimony, and mercury in sediments from Niantic, Norwalk, and New Haven. Squares represent means • comparison intervals. Low- er case letters indicate results of statistical testing.

at the N e w Haven site than the two o ther sites (Fig. 7). T h e m e a n concentrat ions o f PCBs in livers o f winter f lounder increased in the same order as con- centrat ions in sediments; however , no significant dif ferences were found b e t w e e n the levels o f PCBs in the livers o f winter f lounder b e t w e e n sites. At each site, concentrat ions o f PCBs in fish livers and s tomach contents and in infaunal po lychaetes tend- ed to be several-fold h igher than those in sed iments and may indicate b ioaccumulat ion o f these chem- icals.

Sed iment concentrat ions o f chlor inated pesti- cides (CPs) were low ( 3 - 8 ng g- i dry wt) at all sites, and there were no significant dif ferences a m o n g any o f the sites. Similarly, concentrat ions in both s tomach contents , infaunal invertebrates ( 5 0 - 9 0 ng g-] dry wt), and fish livers ( 3 0 0 - 9 0 0 ng g-l dry wt) s h o w e d no between-s i te significant differences. As with PCBs these data suggest b ioaccumula t ion o f CPs.

Trace Metals Mean concentrat ions o f several trace metals (zinc,

lead, copper , c h r o m i u m , mercury , silver, and an- t imony) in sediments were lower in samples f r o m the Niant ic site than those in sediments f rom the o ther s i tes(Figs . 8 and 9). H o w e v e r , no dif ferences were f o u n d in the m e a n concentra t ions o f tin and nickel in sed iment f r o m the Niant ic site c o m p a r e d to the o ther sites. A l t h o u g h m e a n concentrat ions o f most metals were highest at the N e w Haven site, only o n e metal , silver, was significantly h igher at this site c o m p a r e d to the o ther sites. T h e concen- trations o f trace metals in s tomach contents and in liver o f winter f lounder varied considerably a m o n g the sites and appeared unre lated to sed iment con- centrat ions . T h e s e f indings agree with those in oth- er studies (Zdanowicz et al. 1986; Varanasi et al. 1988) where concentrat ions o f trace metals in sed- iment and fish tissue were not correlated.

304 W.D. Gronlund et al.

Sediment Characteristics Two of the factors which influence concentra-

tion of chemicals in sediments are particle size and total organic carbon (TOC). For Norwalk, New Haven, and Niantic, respectively, the percentages of clay/silt were 64, 62, and 82, with the percent- age from Niantic being significantly different from the other sites. Low concentrations of certain chemicals are often associated with low clay/silt percentages (Means et al. 1980). However, in these studies, sediments from Niantic had the lowest con- centrations of most chemicals, they also had the highest proportion of clay/silt. TOC percentages of 2, 3.5, and 0.6 were found for sediments from the Norwalk, New Haven, and Niantic sites, re- spectively. These values were significantly differ- ent between sites, and the low value for Niantic sediments may have had some influence on con- centrations of contaminants.

Discussion Although significantly higher concentrations of

several of the organic chemical contaminants in sediment appeared to be associated with signifi- cantly higher frequencies of several biological ef- fects observed in winter flounder, the cause-and- effect relationships between these effects and con- taminants are poorly understood. Nevertheless, extensive studies in Puget Sound (Malins et al. 1984) on the relationships between chemical contami- nants in sediment and pathological conditions in liver of English sole (Parophrys vetulus) have shown significant relationships between concentrations of AHs and these conditions. In addition, laboratory studies on English sole have demonstrated that ex- posure to extracts of sediment from a contaminat- ed site with high levels of AHs resulted in devel- opment of liver pathology similar to that seen in fish living in association with contaminated sedi- ments (Varanasi 1987). The formation of hepatic DNA adducts has also been demonstrated for both English sole (Varanasi et al. 1989b) and winter flounder (Varanasi et al. 1989c) exposed to extracts of contaminated sediments, specific AHs, and for those collected from contaminated sites in Puget Sound and Boston Harbor.

The concentration of sediment AHs (4,000 ng g-~ dry wt) found at New Haven which appear as- sociated with elevated hepatic disorders and DNA adducts in winter flounder are similar to those re- ported for both Raritan Bay and a site in western Long Island Sound (Zdanowicz et al. 1986). Very similar sediment concentrations of AHs (ca. 5,000 ng g-] dry wt) were associated with elevated fre- quencies of liver pathology in English sole from Elliott Bay, near Seattle, WA (Varanasi et al. 1989a).

Although the concentration gradients for many contaminants generally decrease from west to east (Turgeon and O'Connor 1991), inputs from urban sites within Long Island Sound such as New Haven and Norwalk should not be dismissed. These urban sites have contributed moderately high concentra- tions of sediment contamination even in areas sev- eral miles from sources. Additionally, populations of winter flounder which use areas such as New Haven and Norwalk for seasonal feeding and re- productive activities (represented by those used in these studies) appear to have been deleteriously affected by contaminants.

Conclusions This study has shown that the New Haven site

generally had the highest levels of organic chem- ical contamination of sediment of the three sites sampled in Long Island Sound. The evidence also demonstrated that winter flounder at the New Ha- ven site had the highest frequencies of biochemical and pathological anomalies among the sites. Both DNA adducts and macrophage aggregates appear to be promising measures of effects of contaminant exposure in winter flounder.

None of the sites sampled had contaminant levels as high as the worst conditions previously found as part of the NBSP at other East Coast sites (Zda- nowitz et al. 1986). However, sediment concentra- tions (AHs) at New Haven should be considered moderately high (Turgeon and O'Connor 1991). It should be recognized that the moderately high levels of chemical contaminants (particularly levels of AHs) at the New Haven site were apparently sufficient to have exceeded thresholds for effects, such as hepatic DNA xenobiotic adducts and liver pathology in winter flounder.

ACKNOWLEDGMENTS

Sincere thanks to all of the present and former NMFS En- vironmental Conservation Division staff members who contrib- uted to this study. Especially T. Emry and L. Rhodes for ded- icated service and high quality work during field collections; K. Carrasco for micronucleus evaluations; P. D. Plesha for inver- tebrate collections; Dr. W. L. Reichert for DNA adduct anal- yses; S. Perry for typing; S. Pierce for comparison interval cal- culations and all of the other National Analytical Facility staff for timely and complete chemical analysis. Thanks also to the officers and crew of the NOAA Ship Ferrel especially Cmdr. R. Hunt and Chief Boatswain R. Brinnon for outstanding lead- ership and advice in field operations.

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Received for consideration, April 10, 1990 Accepted for publication, November 1, 1990