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EFFECTS COLD ~ MARINE BENTHIC BIOTA AND COMMUNITIES K. John Scott Science Applications International Corporation ABSTRACT Our understanding of the effects of contaminants on ben- thic organisms lags well behind that for water column species because of the way in which sediments mediate bioavailability and because test protocols using infaunal organism are still in the developmental stage. Although quantitative analyses of benthic communities continue to be a primary assessment tool, their interpretation as to contaminant effects remains diffi- cult, especially under conditions of moderate contamination. It is, therefore, important to determine how sediment contam- inants affect lower levels of biological organization. Con- taminant effects have been described for subcellular, cellu- lar, tissue, whole organism, and population level systems in benthic organisms. The routine application of these responses has been limited, however. There is a critical research need to develop test protocols that address chronic effects and bioaccumulation in both short- and long-lived benthic organ- isms. Such methodologies would allow for the effective inter- pretation of changes in benthic communities in response to contamination and the significance of the community in food chain transfer of sediment contaminants. INTRODUCTION The degree of sediment contamination in our nation's coastal waters has become the subject of intensive research and monitoring programs during the last 10 years. The role that benthic systems play in the sequestering and redistribution of contaminants is now well recognized (Baker, 1980; Dickson et al., 1987~. National and international efforts have sought to document the degree of contamination in sedi- ments and in the associated fauna as a means to rank coastal sites for remedial action (NOAA, 1988; see Marine Pollution Bulletin baselines for examples). Regulatory actions will hopefully control further source inputs to these systems; however, with the ever increasing local ization of population centers along the coastline, determining the con- tribution of nonpoint sources to sediment contamination will remain the biggest challenge. 132 .

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133 Research on the effects of contaminants on benthic organisms lags well behind that for water column species because of the way in which sediments mediate contaminant bioavailability and because test proto- cols using a wide range of infaunal organisms are still in the develop- mental stage. The Environmental Protection Agency's (EPA) sediment quality criteria program is beginning to address the relationship between sediment properties, contaminant availability, and subsequent biological effects (Zarba, 1988~. Approaches to developing these cri- teria rely heavily on acute responses and sediment-water equilibrium partitioning theory. Sediment criteria that depend on acute responses will not, however, provide information necessary to assess chronic, long-term effects that regulate an organism's growth, reproduction, and subsequent function in the benthic community. Although test methods have been developed to assess the effects of water column and sediment associated contaminants on the development of benthic communities (Hansen and Tagatz, 1980), most evaluations of com- munity responses to sediment contaminants are the result of field ben- thic and contaminant surveys. The implications of chemical-specific effects on species abundances and community structure are thus largely correlational. Compounding the problem of determining chronic, popula- tion level effects is the lack of chronic test methodologies using ben- thic species. These tests will be essential to the prediction of con- taminant effects on population abundances and for the interpretation of the significance of community changes. The focus of this paper is to briefly review the types of responses that sediment contaminants have been shown to elicit in macrobenthic communities. Effects at this level of biological organization, how- ever, integrate individual organism and population responses throughout the biological hierarchy. As shown in Figure 1, contaminants can induce effects at any level of biological organization from biochemical or pathological effects to reproduction and population interaction effects (Sheehan, 1984~. The time scales of these effects can vary from hours to years. Therefore, information on the type of response and the life history of the target organisms are necessary for making predictions at the community level. To understand community responses to sediment contaminants, there- fore, a brief review of effects at several levels of the biological hierarchy will be provided. This discussion will follow a summary of the extent of contamination in natural sediments and the bioaccumula- tion of contaminants in benthic organisms. EXTENT OF CONTAMINATION Sediments The most comprehensive assessment of sediment contamination in U.S. coastal waters has been conducted by the National Oceanic and Atmos- pheric Administration's (NOAA) Status and Trends (NS & T) program. Results for benthic and mussel watch sediment surveillance studies from

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135 177 sites are presented in NOAA (1988~. The authors conclude that sil- ver, tin, mercury, and all of the organic compounds are the most repre- sentative of anthropogenic input and that, although there are excep- tions, sediment contamination is most prevalent around urban centers. These studies provide a range of contaminant concentrations for sites not directly influenced by point sources, and thereby reflect basin- or baywide conditions. For the most part, benthic communities at the NOAA NS ~ T sites would be expected to exhibit a range of responses consis- tent with this range of contamination. Where contaminant concentra- tions are at moderate levels, these communities would not be drastic- ally impoverished in either numbers of species or species abundances. Point-source inputs have resulted in many cases in which sediments are much more contaminated than those cited above. Some examples are . New Bedford Harbor, Massachusetts, where PCB discharges have caused sediment PCB concentrations to be in the part per thou- sand range (Weaver, 1984~; Eagle Harbor, Washington, where extremely high aromatic hydro- carbon concentrations (120,000 ng/g) resulted from a creosote wood treating plant (Malins et al., 1985~; Black Rock Harbor, Connecticut, where multiple source inputs have elevated concentrations of PAHs, PCBs, Cd, Cu. Pb and Zn higher than at any NS & T site (Rogerson et al., 19851. The identification of "hot spots" will surely continue as a result of a rising public and regulatory concern about sediment contamination. At sites such as these, the benthic communities are drastically altered and are commonly dominated by contaminant-tolerant, opportunistic species assemblages. TISSUES The bioaccumulation of contaminants from sediment matrices is a com- plex problem that is presently receiving considerable attention in the research and regulatory communities. An understanding of uptake rates of contaminants and the processes regulating bioaccumulation is espe- cially relevant to the establishment of sediment quality criteria. A significant body of literature exists on tissue residue levels in mar- ine organisms based on laboratory and field studies where comparable data are available for sediment concentrations. Most of this literature deals with filter-feeding species, such as the mussel, Mytilus edulis, or with epibenthic forms and bottom- feeding fish that are not in the most intimate contact with the sedi- ments. To assess the mechanisms of contaminant bioaccumulation from sediments, and the subsequent food chain transfer, there is a critical need for studies using infaunal and deposit-feeding organisms. In fact, there is a real technological limitation in the determination of bio- accumulation processes in one of the most important components of benthic communities--the small, fast growing, highly productive oppor- tunistic species of polychaetes, bivalves, and crustaceans. These taxa

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136 are known to be important food sources for demersal fish (Becker and Chew, 1987~. This limitation is due to contaminant detection limits and sample-size constraints associated with these small organisms, many of which are only retained on mesh sizes smaller than 300 ~m. We also know very little about contaminant effects in this group. A general review of metal residues in aquatic organisms can be found in Prosi (1979~. This reviewer and others have observed that there is considerable variation in metal accumulation, even in indivi- duals of the same species found in the same locale (Bradford and Luoma, 19801. This variability primarily results from the differential abil- ity of various species and/or life stages to accumulate, store, and metabolize metal compounds. For example, Bryan (1976) found that the polychaetes Nereis and Nephtys can regulate the uptake of iron, manganese, and zinc, but cannot regulate cadmium, copper, silver, or lead. Crustaceans also are able to regulate copper, manganese, and zinc, but not cadmium (Bryan, 1976~. The ability to detoxify metal compounds (Jenkins and Brown, 1984) may account in large part for the fact that metal bioaccumulation levels are generally found to corres- pond closely the ambient sediment concentrations. Jenkins and Brown (1984) have found that the binding capacity of the organism's metallo- thionein protein pool may be directly related to the metal tissue resi- dues that cause toxic effects. This hypothesis suggests that metals are gradually accumulated to the point where the metallothionein pool is saturated and further uptake "spills over," causing toxicity. The implication of these findings is that there is a small difference between concentrations that have no apparent effect and those causing toxicity. It thus appears that, from a bioaccumulation standpoint, metals do not appear to be a significant problem because toxicity would occur before the bioaccumulation of elevated tissue residues. On the other hand, the accumulation of organic compounds do pose a serious problem because of the affinity of many PAHs and chlorinated organics for animal lipid pools. Although many marine organisms have the ability to metabolize these organic compounds via mixed function oxidase (MFO) systems (Lee, 1984), bioaccumulation, persistence, and the potential for food chain transfer of organics is much more preva- lent than for metals. The uptake of PAHs from water has been well documented, however, uptake from sediments by deposit feeders is not well understood. Available evidence indicates that PAHs are tightly bound to the organic fraction of the sediments and are relatively unavailable for bioaccumulation (Neff, 1985~. Any accumulation would thus result from PAR Resorption from particles to the interstitial water for uptake across the integument or gills. Further compounding the interpretation of PAH residue data is the fact that these contam- inants appear to be rapidly metabolized and detoxified by MFO systems (Stegeman, 1981~. Organochlorine compounds such as PCBs and pesticides tend to be much more persistent in benthic systems (Nimmo, 1985~. The potential for food chain transfer from sediments to deposit-feeding invertebrates to demersal fish has been documented by Goerke et al. (1979) and Young and Mearns (1978~. The level of accumulation of non-polar chlorinated organics in deposit feeders appears to be a function of the organic

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137 carbon content of the sediment and the lipid resources of the organism (Lake et al., 1987~. This hypothesis has recently been tested by Lake et al. (in prep.) using field-collected sediments with a range of sedi- ment PCB and total organic carbon concentrations. Accumulation factors for deposit feeders, when normalized for sediment TOC and organism lipid content, ranged from 2.3 to 7.3. The development and application of this equilibrium partitioning approach is an important component of EPA's program to set sediment quality criteria. SIGNIFICANCE OF CONTAMINATION TO THE BENTHOS BACKGROUND There are many examples from the literature of changes in benthic communities due to contaminated sediments. The most dramatic and clear- cut community changes have been demonstrated for sediments contaminated by oil spills (Sanders et al., 1980; Jacobs, 1980), where there are fairly dramatic shifts in species composition due to immediate acute mortalities and changing recruitment and survivorship patterns. Other examples have been described for sediments with gradients in metal con- centrations (Rygg, 1986~. The most common cases of community effects, however, are those documented for sewage outfalls and other types of organic enrichment gradients (Pearson and Rosenberg, 1978; Stainken, 1984; Swartz et al., 1985b, 1986; Stull, 1986~. Because of the over- whelming multiple effects that organic enrichment may have on community structure (BOD, COD, pH, H2S, CH4) it is often difficult to ascribe community changes to specific contaminants, which may be correlated with a gradient of total organic carbon. The integrated response of the community is most often an after- the-fact assessment of community effects (Sheehan, 1984~. Although it is important to understand the contaminant related processes operating at the community level, it is equally critical to determine the mechan- isms occurring at the individual and population level which are ulti- mately expressed in a community effect. An appreciation of these mechanisms is directly related to a regulatory evaluation of contam- inant effects, as most applicable tests must be conducted at the lower levels of biological organization. In the discussion that follows, I will attempt to illustrate how biological effects at lower levels of organization may influence inte- grated types of responses in benthic populations and communities. I will supplement selected observations from the literature with those drawn from our experience in the Field Verification Program (FVP), a joint effort of the Corps of Engineers (COE) and EPA to evaluate the utility of a variety of biological endpoints as to their effectiveness in predicting the biological effects resulting from the disposal of contaminated dredged materials. The biological responses evaluated in this program included genetic, pathological, physiological, reproduc- tive, population and community endpoints. The sediments that were used in the FVP were dredged from Black Rock Harbor, Connecticut, and disposed of at the COE's dredged material disposal site in Central Long Island Sound. These sediments were contaminated with PAHs (sum = 142,000 ng/g dry), PCBs (A1254 ~ 6,400

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138 ng/g dry), copper (2,900 ~g/g dry), chromium (1,480 ~g/g dry), and cadmium (24 agog dry). Field and laboratory measurements of biological effects were determined over a five-year period, which included both pre- and post-disposal phases. A synthesis of the results of the FVP is provided in Gentile et al. (1988~. INDIVIDUAL RESPONSES Biochemical As discussed earlier, exposure to metals may result in metal binding by proteins and PAH exposure can result in oxidation by mixed function oxidase systems. In their work on metal induction of metallo- thionein and very low-molecular-weight ligands, Jenkins and Sanders (1986) have found correlations between the increased accumulation of cadmium in these pools and growth and reproduction in the polychaete Neanthes. The authors have also observed this relationship for growth in crab larvae. Exposure to crude oil has been shown to induce mixed function oxidase activity in two benthic polychaetes, Capi tella capi tata and Nereis virens . There is some indication that this response may contribute to the relative tolerance of these species, as measured by acute mortality, to oiled sediments. Fries and Lee (1984) suggest that induction of the MFO system in Nereis due to oil expo- sure slows growth and prevents reproduction because of an interference with the normal production of gonadotrophin and own lation-inhibiting hormones. Genetic Genetic studies using benthic invertebrates are rare; a genetic res- ponse has only recently been developed by Pesch et al. (1981), who des- cribed the response, sister chromatic exchange (SCE), in the polychaete Neanthes arenaceodenta. This genetic endpoint was evaluated in the FVP using another polychaete, Nephtys incise . Exposure to Black Rock Harbor sediments did cause an increase in SCE frequency in both laboratory and field exposed worms (Pesch et al., 1988~. The long-term consequences of this genetic response is unknown; however, tumor induc- tion or some other mutagenicity may result. It is clear that these effects are important as genetic polymorphism will enhance adaption to stressed environments. Gras sle and Grassle (1977) have demonstrated that the opportunistic, contaminant-tolerant polychaete Capitella capitata consists of at least six sympatric sibling species. In a separately funded study conducted by the EPA for the National Cancer Institute (NCI), chemical fractions of these same Black Rock Harbor sediments were subjected to three genetic screening assays: the Ames test, the metabolic cooperation assay, and SCE (Gardner et al., 1987~. The latter two tests were conducted using the Chinese hamster V79 lung fibroblasts. The results of all three assays established that these sediments exhibited some form of genotoxicity. Further evidence

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139 of tumor promotion will be discussed below. Pathologies Myers and Hendricks (1985) surveyed the existing literature on path- ological studies with aquatic organisms and found the state of our path- ological mechanisms in this group to be far behind the mammalian coun- terpart. Among aquatic species, the least amount of work has been done on marine infauna. There are several reports that investigated the carcinogenic effects of petroleum hydrocarbons on neoplasia induction in bivalves exposed to oil (Brown et al., 1977; Yevich and Barszcz, 1977; Harshbarger et al., 1979~. Data are beginning to accumulate for bottom-dwelling fish (Malins et al., 1984) that indicate a close assoc- iation between fish diseases and heavily contaminated sediments. Aro- matic hydrocarbons are the most commonly implicated chemicals in these studies. In the FVP, the pathological responses to Black Rock Harbor sedi- ments were examined in four infaunal species: the tube-building am- phipod Ampelisca abdita; the polychaetes NepEtys incise and Neanthes arenaceodentata; and the bivalve Yoldia limatula (Yevich et al., 19861. In A. abdita, Black Rock Harbor sediments caused necrosis of gill epithelia and a loss of normal gill architecture. This species also exhibited atrophied mucous cells and tube glands. These data are con- sistent with observations that Ampel isca builds shorter and more poorly constructed tubes in sediments containing high concentrations of BRH material. Histopathological changes were noted in the epidermis and parapodial muscle of both polychaetes. Mucous-secreting cells were also affected in Neanthes. No pathological effects were observed in Yoldia, which was probably due to a lack of exposure because it would not burrow into Black Rock Harbor sediments. Oysters and flounder exposed to Black Rock Harbor sediments in the NCI study referred to above showed a high degree of pathological abnor- malities (Gardner et al., 1987~. Neoplastic tumors in the oyster were found primarily in the renal excretory tissues, with some tumors found in the gill, gonad, gastrointestinal, heart, and neural tissues . Neo - plastic lesions also developed in the kidney, pancreas and oral epithe- lial surfaces of winter flounder exposed to these sediments. Physiology Physiological measurements, when integrated and expressed as energy balance, have been shown to be sensitive indicators of stress (Bayne, 1975~. This approach has been modified by Gilfillan et al. (1976), who reported a reduced carbon flux in the clam Mya arenaria following exposure to petroleum. Roesijadi and Anderson (1979) developed a con- dition index that varied in concert with the abundance of free amino acids in Macoma inquinata, also exposed to oil-contaminated sediments. Bioenergetic responses of the polychaetes N. incise and N.

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140 arenaceodenta were evaluated with the Black Rock Harbor sediments (Johns et al., 1985; Johns and Gutjahr-Gobell, 1988~. Laboratory expo- sures to mixtures of Black Rock Harbor and control sediments caused reductions in net growth efficiency and scope for growth in each species, respectively. Respiration and excretion rates in NepEtys collected from the disposal site were lower than the same rates in worms collected from control areas. Responses of this nature may explain why the eventual growth and population size of this species was impacted at the FVP disposal site. Behavior A behavioral response is, for mobile organisms, the first line of defense against exposure to a heavily contaminated sediment. Avoidance of noxious sediments is also a common response of infaunal benthic invertebrates (Swartz, 1987) and this parameter has been incorporated into sediment toxicity tests with amphipods (Swartz et al., 1985a). Other behavioral responses in benthic invertebrates are generally difficult to describe because of observational problems associated with the sedimentary medium. Behavioral effects were observed in the studies with Black Rock Harbor sediments. The amphipod Ampelisca showed a distinct emergence response to these sediments. The bivalve Yoldia fai led to burrow into any Black Rock Harbor mixtures greater than 50 percent and, when pushed into the sediments, would not feed. The burrowing activities of Nephtys were also altered, such that it would only create its burrows in sediment layers without Black Rock Harbor material. The implications of changes in burrowing behavior are twofold. Inability to rebury into contaminated sediments makes the organism susceptible to predation (Pearson et al., 1981~. It also disrupts regular feeding behavior for deposit feeders affecting ontogenetic growth and the normal organism-sediment interactions. Growth and Reproduction Growth and reproduction are two very closely linked processes, es- pecially as related to individual maturation rates and attainment of reproductive age or size. All of the responses discussed above can sig- nificantly affect growth rates by impairing feeding mechanisms, food assimilation and the conversion of energy resources into body tissues. Regardless of the mechanism, the end result will be slower growth and maturation rates. The results of several studies examining the effects of heavy metals and petroleum hydrocarbons on reproduction in benthic poly- chaetes have been summarized by Reish (1980~. In these water-only exposures, all species showed reproductive effects to all compounds; however, the relationship of these effects to sediment contamination is uncertain because the organisms were not exposed to the contaminants in sediments. Similarly, Jenkins and Mason (1988) have demonstrated

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141 growth and reproductive effects in Neanthes as a result of water column cadmium exposures. A series of chronic experiments were conducted for the FVP using A . abdi ta exposed to suspended Black Rock Harbor sediments (Gentile et al., 1985, 1987; Scott and Redmond, in press). Long-term exposures to these sediments caused significant reduction in the mean size of this amphipod in all Black Rock Harbor treatments. The most critical growth reduction occurred with the female amphipods. Because they grew slower and matured later, time-specific fecundity was reduced. Exposed females also produced fewer eggs because they were smaller. Growth in the polychaete N. incise, was also impaired by exposure to Black Rock Harbor bedded sediments, probably as a result of its inability to create burrows and effectively feed in these sediments (Johns et al., 1985). Survival Acute mortalities resulting from exposure to contaminated sediments under laboratory conditions have been well documented (Swartz, 1987~. This response continues to be one of the primary tools used to evaluate the relative toxicity of sediments. In general, crustaceans--particu- larly amphipods--have been shown to be the most sensitive group. This was the case in the FVP where A. abdi ta's acute and chronic res- ponses were the most sensitive of 11 species tested. Chronic survival studies with benthic species and contaminated Seder meets are rare because of a paucity of chronic test methods. Survival of benthic species are usually inferred from population abundance com- parisons among contaminated and noncontaminated field sites. Differen- tial survival among the species in the community is one of the primary mechanisms leading to shifts in community dominance and diversity. POPULATION AND COMMUNITY LEVEL RESPONSES The Successional Paradigm The response of soft-bottom benthic communities to pollutant stress was extensively reviewed by Pearson and Rosenberg (1978) who suggested a model for community recolonization and succession following distur- bances due to anthropogenic influences. Rhoads et al. (1978), in the evaluation of community changes following dredged material disposal, recognized similarities in the types of species that were dominant at various stages of the recolonization process. Based upon the work of McCall (1977) and Pearson and Rosenberg (1978), they identified two distinct stages of succession, each typified by species with certain life history characteristics. The stages of succession and their relation to sediment processes are illustrated in Figure 2. The first stage is characterized by small tube - dwelling polychaetes or oligochaetes who are short lived, opportunistic species. They are either suspension or deposit feeders

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142 and they have little contact with deeper subsurface sediments. These species are progressively replaced by an intermediate assemblage consisting of shallow-dwelling bivalves or tubicolous amphipods. The final stage, or equilibrium assemblage, is dominated by infaunal deposit feeders who are large, long-lived, and feed deep in the sediment. As can be seen in Figure 2, this progressive infaunalization increases sediment bioturbation and particle mixing and, hence, pore water exchange at the sediment- water interface. Population and Community Responses to Contamination Rates of population growth were predicted for two infaunal species in the FVP. Assessments of Nephtys population growth were A : · ; · · i, anaerobic mini ment ~ ,\ ? _-; ~ OxidIzed sediment ~ I ~~ ^~-i-.i dIstUr - ~ B fiber blanket W8t~f k - ..^,'~:~;~ ~ ~ . ~ ~ . ~ ~ ~ - ~14 _O FIGURE 2 A. Development of organism-sediment relationships over time following a physical disturbance in Long Island Sound. B. Organism- sediment relationships associated with pollution gradient due to pulp mill effluent (Pearson and Rosenberg, 1978~. SOURCE: Rhoads and Germano, 1982. 1_3

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FIGURE 3 Species-abundance- biomass diagram of faunal change along a gradient of organic enrichment in Loch Creren. SOURCE: Pearson, 1981. FIGURE 4 Abundance changes of some dominant species along an enrichment gradient in Loch Creren. SOURCE: Pearson, 1981. 144 3 o ,, 1000 ~ . In C) Z to 100— : 2 10 ~ E f fluent Point ._ Increasing D'stonce From Outfall 50 0 ~ 5000 Or\ /' '\ m - 40 _ - 4000 1 \ . t \\ 3 -30- ~3000 1 /~_~_~ ~ - - 20 ~ 2000 1 1 ~ 5 - 10 - 1000 / / ~ F 20 G20 Z 20 ~ 20 Station plumber r\ 2SO 200 150 100 50 120 K20 CAPtrELLA SCOLELE P.S ~ ~ SC~LtBREG | i~ ~ELINNA ~ ~ CORSULA - - - ~ // ~>~ I I ~ ~ 1 SO 100 200 3S0 600 8SO INSTANCE fRO~ O[J7FALL ( m ) The following discussion will describe, in some detail, our studies on the benthic community recolonization process resulting from the dis- posal of Black Rock Harbor sediments at the FVP disposal site (Scott et al., 1987~. The recolonization process was measured by documenting the rate of recolonization of the disposal site and comparing this with the ambient (control) community. The parameters used to describe recoloni- zation and convergence with the predisposal system were species num- bers, abundance of numerically dominant species, degree of infaunaliza- tion (successional stage), and depth of biogenic mixing of the bottom sc KNELLS NEp~r~ys

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145 sediments (another measure of infaunalization). The latter two param- eters were described using the REMOTSR interface camera (Rhoads and Germano, 1982~. The benthic community, sampled at four stations at the FVP site on an easterly transect, prior to disposal (baseline) and off the disposal mound for six months following disposal, was dominated by a subsurface infaunal deposit- feeding assemblage consisting of the protobranch bi- valves Nucula annulata and Yoldia limatula and the polychaete worm Nephtys incise. All three of these organisms are Stage III taxa (sensu Rhoads and Germano, 1982) that have mean life spans greatly exceeding one year. Reproduction may take place two or more times per year. They are important in bioturbating the sediment column to a depth of approximately 4 cm; this biogenic mixing controls both pore water and solid-phase chemistry. This subsurface deposit-feeding assemblage was overlain by near-surface populations of the deposit-feeding polychaetes Mediomastus ~mbiseta and the suspension-feeding mactrid bivalve Mulinia lateralis. These latter two species are well known members of Stage I series representing opportunistic adaptive strategies. Mean life spans are less than one year and reproduction of the population occurs several times per year. The sympatric association of opportun- istic colonizers (Stage I taxa) with longer-lived species (Stage III taxa) is common in estuaries and embayments. This assemblage type has been previously described for the CLIS silt-clay facies (Sanders, 1956; Michael, 1975) and for the silt-clay basinal facies of Buzzards Bay (Sanders, 1958~. The temporal pattern of recolonization consisted of two separate processes operating at different time scales. The first process was the immediate recolonization of the dredged material mound, which occurred during the first six months following disposal. Short-lived, relatively tolerant, early colonizing species, Polydora and Mulinia, populated the mound in significant densities, and in some cases were most abundant on the mound apex. This phase of the recolo- nization of the FVP site was not unlike that seen for other disturbed sites within Long Island Sound and elsewhere (Rhoads et al., 1978~. The greater abundances on the mound are not surprising since many early colonizers thrive in disturbed bottoms where the surface sedi- ments contain high inventories of labile organic matter (Rice and Rhoads, 1988~. In defaunated habitats (McCall, 1977), neither competi- tion for space nor the biologically mediated geochemical conditions of the sediment would pose problems for recruitment. In fact, the appear- ance of sedimentary sulfides at the surface may stimulate settlement in some opportunistic species (Cuomo, 1985~. The second component of the recovery process, which may begin con- currently with the initial colonization, is the progressive development of subsurface bioturbation associated with the re-establishment of the long- lived species . The time scale of this process may be on the order of one to two years or more. It was not until 19 months after disposal that head-down feeding voids were observed on REMOTSR images at the FVP site mound stations, even though the major frequency mode of the Bio- logical Mixing Depth (BMD) at those stations had converged with that of reference site within one year. The mound station continued to have a

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146 significantly lower BMD even though head-down deposit feeders from the ambient community were among the recolonizers. - Both Nephtys and Yol die experienced some recolonization of the mound stations during the first six months following disposal. Gradual recruitment of these species occurred during the next 18 months, until population densities approached those at the reference station. The recolonization pattern for Yoldia and Nephtys showed that the mound was recovering and converging with the ambient sea- floor. The size structure of the Nephtys population was, however, not similar to that of off-mound stations in that these worms were significantly smaller (Zap ac and Whitlatch, in press). The proto- branch Nucul a did not recolonize the mound in significant numbers. At the mound apex the lack of recruitment was likely related to the presence of a large sand fraction (1 to 3 cm deep). Nucula is also absent from other sand-covered disposal mounds in CLIS. Recent analyses of grab samples collected at a mound station without a sand lens show that Nucula have been unable to colonize the fine sedi- ments at this station, indicating a toxic effect on this species (Scott, unpublished data). The failure of the ambient Stage III assemblage (Nephtys , Nucula, and Yoldia) to become fully established on the mound after two years may have been due to grain-size effects, as other deep bioturbating organisms were present, although in low densities. It may be that the sand lens on the surface of the mound was effectively capping the sub- surface contaminated BRH sediments. As a result, when the headdown feeders grew to a size where feeding depths penetrated the subsurface contaminated silts, feeding activities and survival may have been im- paired. The physiological and pathological studies with Nephtys, and the behavioral observations on both Nephtys and Yoldia would support this conclusion. IMPLICATIONS OF CHANGES IN COMMUNITY STRUCTURE Alterations in the species composition, abundance, and diversity of benthic communities have two primary affects on the broader ecosystem: 1. influences on higher trophic levels and habitat resource value, and 2. influences on sediment processes and biogeochemical cycling. These processes have been summarized in Swartz and Lee (1980), Lee and Swartz (1980), and are described in Table 1. Boesch (1982) has reviewed the trophic interactions between soft- bottom benthic communities and bottom-feeding fish in the New York Bight. In examining changes in community structure in silt-clay facies, it is clear that responses to disturbance during the colonizing phase involve a shift from subsurface, deposit-feeding species to those inhabiting and feeding on surface sediments and suspensions. It has been shown that dense populations of these tolerant species can limit recruitment of other organisms by direct predation on settling larvae.

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147 TABLE 1 Benthic Ecosystem Attributes Associated with Pioneering and Late S tage Series Successional stage System attribute Early (Stage I) Late (Stage III) Secondary production Prey availability High potential for r- selected taxa High--prey are concen- trated near surface Potential for food- Highest for suspended web contamination or recently sedimented particulates. Body burdens may be low re- lated to short mean life spans C ontaminant/nutr i ent recycling Potential for bottom- water hypoxia Limited to solutes in c 3 cm High--storage systems for labile detritus Lower potential for K- selected taxa Lower--infauna are deep burrowings Highest for deeply buried contaminants. Longer mean life spans may lead to significant body burdens Solutes exchanged over distances to 20 cm or deeper Low--a recycling or "purging" system NOTE: aNonlethal predation of distal ends of siphons or caudal segments may be important for some predator species. SOURCE: Rhoads and Germano, 1986. These early stages are typically characterized as having high abun- dance, biomass, and secondary production. This assemblage, predominating the sediment surface, is much more available to bottomfish as a food source (Becker and Chew, 1987~. Because this group of species is the first to colonize contaminated sediments, the potential for food web contamination needs to be ad- dressed. The small size, rapid turnover, and high production rates make these organisms an excellent food source for fast growing juvenile fish. The short life spans of colonizing species would indicate that bioaccumulation under these conditions may not be a problem, but that has yet to be determined. The distribution of sediment contaminants and nutrients is also altered by shifts in community structure and composition. Shallow- burrowing forms will only affect transport over the top few centimeters and, as the RED rebounds toward the sediment-water interface, anoxic conditions in the deeper layers would more tightly bind some contaminants. As colonization progresses, this condition would undergo reversal .

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148 Another effect of changes in species composition is an alteration in habit structure (Lee and Swartz, 1980), particularly in the surface sediments. Formation of dense tube mats can significantly influence hydrodynamics and surface flow characteristics of the boundary layer which have been demonstrated to increase sedimentation rates (Rhoads and Bayer, 1982~. Changes in the grain-size distribution can also result from extensive pelletization of the surface sediments (Cuomo and Rhoads, 1987~. These factors can restructure the composition of surface sediments which may ultimately affect larval recruitment of benthic species. CONCLUS IONS AND RECOMMENDATIONS The effects of sediment contamination on changes in benthic commun- ities have been largely determined through correlational analyses. There are few laboratory studies directly linking a sediment contamin- ant to community effects (e.g., Tagatz, 1983), and we are left with the problem of attempting to interpret community change and the relative importance of sediment contaminants as a cause of that change. Sedi- ment physical properties and biological interactions must also be fac- tored into these interpretations. Benthic communities show responses to sediment contamination under severe contaminant stress. Locations exhibiting these conditions are prime candidates for remedial action. The larger issue requiring atten- tion, however, is the long-term, low-level contaminant input to coastal systems and the resultant subtle changes in species composition and abundance. Given our inability to discriminate between contaminant effects and natural variability, these types of changes are most likely going unnoticed. The major contaminant inputs and sediment contaminant impacts occur on coastal systems, many of which are in estuaries. In their review of stress effects in benthic communities, Boesch and Rosenberg (1981) sug- gest that estuarine organisms are more resistant to stress than are those in more stable environments, e.g., the deep-sea. They relate this observation to the ability of estuarine and nearshore fauna to tol- erate a wide range of environmental factors, such as salinity, tempera- ture, and suspended solids. This tolerance has selected for a suite of species that are opportunistic, have high turnover rates, and contrib- ute to the extremely dynamic nature of nearshore biological systems. The variable recruitment and distribution patterns of these species contribute to the difficulty in understanding contaminant effects. It appears that these opportunists are capable of adapting to contaminant stress, but the costs to the organism, in terms of long-term population consequences, are largely unknown. The significance of bioaccumulation in this group and, subsequently, in the food chain transfer of contami- nants is also unclear. The effects of the long-term degradation of benthic systems and the ability of benthic organisms to adapt to this chronic stress is a criti- cal factor in the management of point- and nonpoint- source discharges . As such, there is a pressing need for the development of laboratory

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149 test systems to evaluate this chronic stress in benthic organisms. This effort should concentrate on chronic level effects and on - bioaccumulation studies with both opportunistic and longer-lived deposit feeders. The methods should have the ability to predict such effects under field conditions and be able to predict linkages between lower and higher levels of biological organization. As the data base on these effects grows, our ability to interpret subtle community changes will increase dramatically. ACKNOWLEDGMENTS Support for the preparation of this paper was partially provided under EPA contract #68-03-3529 to Science Applications International Corporation. Dr. Donald Rhoads ' (SAIC) review of the manuscript is appreciated. The contents of the manuscript do not necessarily reflect the views or policies of EPA. Nor does the mention of trade names constitute endorsement or recommendation for use by EPA REFERENCES Baker, R. A. 1980. Contaminants and Sediments. Ann Arbor, Mich.: Ann Arbor Science Publishers. Bayne, B. L. 1975. Cellular and physiological measures of pollution effect. Mar. Poll. Bull. 16:127-128. Becker, D. S. and K. K. Chew. 1987. Predation on Capitella spp. by small-mouthed pleuronectids in Puget Sound, Washington. Fish. Bull. 85:471-479. Boesch. D. F. 1982. Ecosystem consequences of alterations of benthic community structure and function in the New York Bight region. In Ecological stress in the New York Bight: Science and Management, G. F. Mayer, ed. Columbia, South Carolina: Estuarine Research Federa- tion. Pp. 543-568. Boesch, D. F. and R. Rosenberg. 1981. Response to stress in marine ben- thic communities. In Stress Effects on Natural Systems, G. W. Bar- rett and R. Rosenberg, eds. New York: John Wiley and Sons. Pp. 179- 200. Bradford, W. L. and S. N. Luoma. 1980. Some perspectives on heavy metal concentrations in shellfish and sediment in San Francisco Bay, Cal - ifornia. In Contaminants and sediments: Volume 2, R. A. Baker, ed. Ann Arbor, Mich.: Ann Arbor Science Publishers. Pp. 501-S32. Brown, R. S. , R. E. Wolke, S. B. Saila, and C. W. Brown. 1977. Preva- lence of neoplas ia in 10 New England populations of the soft shell clam Mya arenaria) . Ann. N.Y. Acad. Sci. (1977b) 298:522-534. Bryan, G. W. 1976. Some effects of heavy metal tolerance in aquatic organims. In Effects of Pollutants on Aquatic Organisms, A. P. M. Lockwood, ed. Cambridge, England: Cambridge University Press. Pp. 7-34. Cabioch, L., J.-C. Dauvin, and F. Gentile. 1978. Preliminary observa- tions on pollution of the sea bed and disturbance of sublittoral

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