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OCR for page 132
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
.
OCR for page 133
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
OCR for page 134
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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
OCR for page 136
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
OCR for page 137
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
OCR for page 138
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
OCR for page 139
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.
OCR for page 140
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
OCR for page 141
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
OCR for page 142
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
:
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anaerobic
mini ment
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OxidIzed
sediment
~ I ~~
^~-i-.i dIstUr - ~
B
fiber blanket W8t~f
k - ..^,'~:~;~ ~ ~ . ~
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- ~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
OCR for page 144
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
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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
OCR for page 149
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
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Representative terms from entire chapter:
rock harbor
