U.S. Geological Survey Toxic Substances
Hydrology Program--Proceedings of the Technical Meeting, Colorado Springs,
Colorado, September 20-24, 1993, Water-Resources Investigations Report 94-4015
Challenges in Detecting Contaminant Effects on an Estuarine
Ecosystem Affected by Many Different Disturbances: San Francisco Bay
Samuel N. Luoma (U.S. Geological Survey, Mail Stop 465, Menlo
Park, Calif. 94025) and Frederic H. Nichols (U.S. Geological Survey, Mail
Stop 465, Menlo Park, Calif. 94025)
The Suisun Bay/Delta at the head of San Francisco Bay is an area where
complex factors converge to affect the success of aquatic species. Water
diversion and drought have reduced river flows to the bay. The historic
elimination of marshes has permanently removed an important source of carbon
while river diversion and drought have reduced river-borne inputs of carbon.
The invasion of the bay by an exotic clam has affected the abundance of
other benthic species and has eliminated previously observed phytoplankton
biomass peaks. Coincidentally, populations of important resource species
have declined. Persistent contamination in Suisun Bay/Delta accentuates
the adverse effects of the above first-order problems. Selenium contamination
in benthos is sufficient to affect upper-trophic-level organisms such as
birds and fish. Pulse inputs of pesticides occur during high flows. Locations
in Suisun Bay were identified that are chronically contaminated with trace
organic compounds, cadmium, chromium, and vanadium. At these locations resident
bivalves are in poorer condition and have modified reproductive cycles,
compared to elsewhere in the estuary. Long-term studies are allowing identification
of the relative importance of different factors that disturb biological
processes in the estuary. Few multi-disciplinary, long-term field studies
are conducted in environments modified by human disturbance. Results from
Suisun Bay show how continuity in the study of cause-and-effect may be the
only way to separate the influence of the myriad of processes that contribute
to ecological characteristics in estuaries.
The array of human activities that have disturbed the San Francisco Bay
ecosystem since the gold rush of 1849 are well known (Nichols and others,
1986). However, the effects and relative importance of specific activities
are not as well understood.
One focus of the initial phase of the San Francisco Bay toxics program
has been the characterization of contamination and its effects in the context
of the myriad other disturbances that affect the Suisun Bay and Delta region.
In this paper we discuss recent progress in studies of both the natural
variability of the Suisun Bay/Delta and effects on aquatic life of human-induced
stresses including contaminants.
RIVER FLOW AS A MAJOR DETERMINANT OF ECOSYSTEM
The upper San Francisco Bay is a complex estuarine system bounded on
its landward side by a tidal freshwater Delta, a highly dissected region
of channels and islands at the mouths of the Sacramento and San Joaquin
Rivers. The rivers converge at the eastern end of Suisun Bay, an important
nursery area for estuarine fish populations.
Flow from the Sacramento and San Joaquin river system, draining about
40 percent of the land area of California, reflects both the pattern of
precipitation over western North America and the operation of the world's
largest man-made water management system (Peterson and others, 1989). More
than half of river water flowing toward San Francisco Bay is diverted from
the drainage basin through impoundment of snowmelt in reservoirs and pumping
of Sacramento and San Joaquin river water from the Delta. The diverted water
is consumed in irrigated agriculture and by urban and industrial uses both
within and beyond the Bay's watershed (Nichols and others, 1986). The result
is greatly reduced flows into the estuary during spring.
Despite the large-scale water diversion, the estuary typically receives
large annual winter/spring pulses of freshwater runoff. Since 1984, however,
persistent drought combined with the continuing water diversion to virtually
eliminate the annual pulses of freshwater except for an exceptional flood
during the spring 1986 (fig. 1).
Figure 1. Monthly average discharge of the Sacramento River at
Chipps Island in San Francisco Bay.
The reduced flow of freshwater into the estuary has contributed
to major changes to the Bay's ecosystem. As an example, striking
declines in the abundance of a number of aquatic species
were observed over the last several decades (Jassby and others,
1993a). The mechanisms differ, but reduced river flow seems
to have affected the success of a native species of zooplankton,
the local mysid shrimp, striped bass, smelt, flounder, and mollusks
that inhabit Suisun Bay (Jassby and others, 1993a). The
freshwater/seawater interface, as indicated by the geographic
location of the 20/00 isohaline in bottom water, has moved
upstream to the detriment of the freshwater organisms that inhabit
the region. The reduced flows and upstream movement of salt also
have increased the exposure of fish populations to the diversion
pumps in the Delta where huge numbers of fish are lost
(Jassby and others, 1993a).
Recent studies have demonstrated that reduced river flow also has caused
a reduction of organic carbon inflow into the estuary (Jassby and others,
1993b). This work demonstrated that San Francisco Bay has a low input of
organic carbon compared to that of many other estuarine systems (Jassby
and others, 1993b). Poor light penetration into the silt-laden waters of
the Bay limits in situ carbon production by phytoplankton and vascular plants.
The extensive marsh system that once existed was also largely eliminated
early in this century, reducing carbon inputs from what was once a major
source. Thus the rivers are now the remaining important source of carbon
input to Suisun Bay/Delta. As river flow was reduced by drought and water
diversion, carbon input was reduced concomitantly. The application of isotopic
and molecular tracers has revealed that an important source for the organic
matter now supporting benthic organisms in the upper estuary is freshwater
algae produced in the rivers and Delta (Canuel and others, in preparation).
This contrasts to South San Francisco Bay where in situ production is most
important (Jassby and others, 1993a).
Another important change in the estuarine ecosystem since the onset of
the drought is the disappearance of the summer phytoplankton biomass maximum
that typically appeared in the Suisun Bay region (Alpine and Cloern, 1992).
This is likely the result of drought-related increases in the abundance
of estuarine benthic suspension-feeding organisms, particularly that of
a recently introduced Asian clam.
EFFECTS OF AN EXOTIC SPECIES
Historically, the most pronounced change to the benthic biota of San
Francisco Bay has come from the accidental and intentional introduction
of exotic species. Large numbers of sediment-dwelling invertebrates were
first introduced during the latter half of the 19th century with live oysters
that were shipped by train from East coast estuaries and transplanted in
the bay (Nichols and others, 1986). Exotic invertebrates continue to arrive
in the bay in ballast water of cargo ships.
A recent arrival from the estuaries of east Asia, the clam Potamocorbula
amurensis, has been remarkable in the rapidity with which it became
the numerically dominant species throughout the northern part of the estuary
and in its potential to change food-web processes (Carlton and others, 1990).
Potamocorbula arrived in San Francisco Bay immediately after the
major flood of 1986 when most of the estuarine benthic invertebrates were
eliminated from the upper estuary because of their intolerance to fresh
water. Within months of its first detection in October 1986, Potamocorbula
became the most abundant benthic organism in Suisun Bay, and has prevented
the bottom dwelling species that once dominated during low flow conditions
(for example, Mya arenaria) from recolonizing the area (Nichols and
others, 1990) (fig. 2). The combination of its great abundance and the efficiency
with which it filters food particles from the water column has resulted
in the near elimination of phytoplankton (diatoms and other microscopic,
single-celled plants that form the base of aquatic food chains) from the
water of the Suisun Bay region (fig. 2; see Alpine and Cloern, 1992). Further,
there is laboratory evidence that Potamocorbula eats the juvenile
stages of some zooplankton, possibly contributing to the reductions in zooplankton
abundance noted during the prolonged drought (Obrebski and others, 1992).
Figure 2. Annual discharge of the Sacramento River in cubic meters
per second (solid line), concentrations of chlorophyll a in milligrams per
cubic meter (line through open squares), and abundance of the clams Mya
arenaria (solid bars) and Potamocorbula amurensis (striped bars)
in Suisun Bay expressed as number of individuals per meter squared, between
the years 1974 and 1992.
The population biology of Potamocorbula has been intensively studied
in Suisun Bay, San Pablo Bay and South Bay in monthly samplings between
1989 and the present. Genetic studies (electrophoretic separation of isozymes)
indicated Potamocorbula had an unusually high within-population genetic
variability, contributing to its ability to survive in a range of estuarine
conditions (Duda, 1993). A study of its reproductive activity throughout
the Bay, under varying salinity, temperature and food regimes, demonstrated
major differences in reproductive seasonality between north and south Bay.
The animals from Suisun Bay were reproductively active during shorter periods
than elsewhere. This difference coincided with, and thus may be related
to, spatial differences in food availability and osmotic stress, or possibly
contaminant stress. Age structure and condition index (tissue weight of
a bivalve of a given shell length) differed among stations in Suisun Bay,
and between Suisun and other parts of the estuary. Clams from the upper
end of Suisun Bay were generally of longer shell length, had a lower condition
index and demonstrated less seasonal fluctuation in condition index than
elsewhere (Brown and Luoma, in preparation). Again it is not yet clear whether
this is a response to reduced food availability or higher contaminant exposure.
TRACE ELEMENT CONTAMINATION
It is probable that contamination from anthropogenic waste discharges
is contributing to some of the ecological changes occurring in the upper
San Francisco Bay estuary, and biological differences between Suisun Bay
and other regions. Recent results of the analysis of sediment cores from
San Francisco Bay indicate sediments and water have been contaminated for
decades by potentially toxic trace metals (Hornberger and others, in preparation;
Van Geen and others, in preparation) and trace organic contaminants (Pereira
and others, in preparation; Hostettler and others, in preparation). Industrial
and urban development coincided with increased sedimentation during the
last 40 years (Fuller, in preparation) and enriched concentrations of Cu,
Ag, Pb and Zn. Sediments contaminated for more than one meter in depth are
found from Suisun Bay to Richardson Bay, near the Golden Gate. Pesticides
(predominantly DDT) and petroleum by-products are enriched to this depth
in Richardson Bay sediments.
The Suisun Bay/Delta was characterized by Biggs and others (1989) as
one of the estuaries in the United States most susceptible to pollution
impact because the physical characteristics of this system limit its natural
resilience. River-transported metals, and wastes form nine of the largest
point source dischargers in the Bay area are released directly into Suisun
Bay (Luoma and others, 1990).
Recent USGS studies illustrate some characteristics of modern organic
and inorganic contamination in Suisun Bay. Water soluble pesticides occur
periodically in detectable concentrations in Suisun Bay when runoff from
agricultural fields reaches the estuary (Kuivila and others, 1996). These
pulse inputs from winter storms are superimposed on chronic contamination
with petroleum by-products (Pereira and others, 1992) and trace elements
(Luoma and others, 1990; Johns and Luoma, 1988; Luoma and others, 1992;
Brown and Luoma, in preparation).
Selenium is an example of a chronic contaminant. Field surveys and mass
balance calculations (Johns and Luoma, 1988; Cutter, 1989) demonstrated
that the most important sources of Se are industrial discharges located
near Carquinez Strait. During the low river flows characteristic of the
estuary since 1986, Se enrichment in water, suspended particles and benthic
species spread throughout Suisun Bay. Substantial Se contamination is found
in large fish and in diving ducks in Suisun Bay. The concentrations of Se
in water are well below those that cause toxicity in bioassays, but Se concentrations
in clams (the food of diving ducks and some fish) are at the level that
causes toxicity to birds and fish in food. The combination of studies showed
that the contamination of the upper trophic level organisms, and the concomitant
threat to their health, resulted from highly efficient transfer of selenite
(the form of Se discharged by industry in the area) from water, to phytoplankton
and then to clams via ingestion of phytoplankton (fig. 3).
Figure 3. An illustration of the concentrations of selenite in
micrograms per liter, selenium in suspended particles in micrograms per
gram, selenium in clams in micrograms per gram, and the toxicity of selenium
in the food of ducks typical of Suisun Bay.
Analysis of Potamocorbula tissues has been employed to define
chronic trace metal contamination, in addition to selenium. The abundance
of this clam across across a broad range of salinities in the system makes
it an especially suitable organism for spatially comparative studies of
contamination. Laboratory studies also showed that P. amurensis rapidly
bioconcentrates metals in its soft tissues from both food and solution (Brown
and Luoma, 1995; Decho and Luoma, 1995). Potamocorbula were sampled
and analyzed monthly at six stations between January, 1991 and April, 1992,
a period of relatively stable river flow. Thus, influences of physical and
salinity variability on assessment of source inputs was minimized. A consistent
spatial gradient in enrichment with Cd, Cr, Ni, and V was observed in the
clam tissues (fig. 4). Concentrations were highest in upper and mid-Suisun
Bay and declined through Carquinez Straits into San Pablo Bay. All metals
except silver were more enriched in Suisun Bay than in South Bay. The same
general gradient in contamination was observed at every sampling time through
the 14 month period. Interestingly, the highest concentrations of metals
were found in Honker Bay, where no immediate point sources of metal input
occur. These data raise the possibility that Honker Bay could be a depositional
zone for upper Suisun Bay. Hydrodynamic studies will aid an evaluation of
Figure 4. Distribution of chromium concentrations in tissues of
the clams Potamocorbula amurensis and Corbicula fluminea in
the San Joaquin River, Suisun Bay and San Pablo Bay.
INTERACTION OF CONTAMINANTS WITH OTHER DISTURBANCES
The gradient of chronic contamination in Suisun Bay coincides with some
of the unique biological characteristics of the area. In P. amurensis
these include the gradient of lower condition index in Suisun Bay to higher
condition index in San Pablo Bay, the lack of a seasonal cycle of condition
index in Suisun Bay, and the spatial differences in the seasonality of reproduction
in the species. A decline in the condition of a bivalve and alterations
to reproductive capabilities can be symptoms of stress in bivalves. Trace
elements can cause these responses by disrupting the energetic balance of
the organism and reducing energy available for reproduction and growth (Widdows,
1985). On the other hand, food availability and other natural or anthropogenic
disturbances can also cause such changes or interact with contaminants in
complex ways to produce responses of communities, populations and individuals
(Luoma and Carter, 1991).
Ecologists typically cite natural processes or anthropogenically induced
changes in habitat conditions to explain differences in populations or declines
in fisheries. Toxicologists often search for effects of contaminants where
waste discharges from human activities impinge on an aquatic environment.
Sufficiently careful, detailed ecological studies that consider contaminants
as one of several variables of influence are rare. The studies of 1989 -
1993 identified and specifically characterized ecological and biological
anomalies in Suisun Bay. These studies identified several processes that
could cause those anomalies, including reduced river flow, lowered carbon
inputs, changes in water column ecology caused by invasion of an exotic
species, and persistent contamination. Continuity in collection of data
that describe these processes, including time series that extend for decades,
have previously provided opportunities to distinguish the relative importance
of different processes in complex estuarine environments (Jassby and others,
1993a; Nichols and others, 1986). This same approach is the best approach
to distinguishing factors that control ecological and biological processes
in Suisun Bay.
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