Introduction
For
over three decades, sand-sized protozoans known as foraminifers
have made contributions to our understanding of environmental problems
in urban areas (Alve, 1991; Clark, 1971; Ellison et al., 1986; Watkins,
1961). Benthic foraminiferal assemblages are particularly sensitive
pollution indicators in estuarine and coastal areas (Alve, 1995)
because they vary spatially and temporally in relation to environmental
variables and can respond to almost imperceptible physical change
in the environment due to pollutants. Foraminifers also have similar
distributions to those of shallow marine invertebrates (Buzas and
Culver, 1991, 1993), and can therefore act as proxies for larger
organisms in polluted environments. In addition, the ability of
foraminifers to respond to environmental degradation is enhanced
because they reproduce quickly, as often as every three months to
one year (Murray, 1991).
Benthic
foraminifers are also useful in environmental studies because they
are easily acquired, since they live primarily in the uppermost
centimeters of sediment (Buzas, 1977; Collison, 1980) and are very
abundant in marine and estuarine habitats (Buzas, 1978; Lankford,
1959); one study estimated that the maximum foraminiferal density
at a single site was greater than 4 million living individuals per
square meter with a sediment thickness of 1 cm (Sen Gupta, 1971).
As primary consumers, foraminifers occupy a position near the bottom
of the trophic structure of marine and estuarine communities, making
them critical components of many, if not all, food chains (Lipps,
1983; Lipps and Valentine, 1970). They feed on items which cannot
be utilized by most larger invertebrates, such as diatoms, bacteria,
nannoplankton, detritus, small arthropods, small sea urchins, and
other foraminifers (Lipps, 1983; Lipps and Valentine, 1970; Murray,
1991). They, in turn, are eaten by copepods, planktonic larvae,
crabs, worms, scaphopods, shrimp, gastropods, fish, and other foraminifers.
Any change at this low trophic level due to environmental degradation
is worth investigating because it may subsequently be transmitted
up the food chain.
The
response of foraminiferal assemblages to industrial and municipal
pollution has been documented in San Francisco Bay (van Geen et
al., 1993) and in many other areas, including Southern California
(Bandy et al., 1964a, 1964b, 1965a, 1965b; Seiglie, 1968; Watkins,
1961), the eastern United States (Ellison et al., 1986), and in
many other countries (e.g., Canada, Norway, England, the Mediterranean,
and the Caribbean). These and other studies have shown that the
distribution of benthic foraminifers is affected by organic enrichment
of the sediments, increased heavy metal loading, and other anthropogenic
contamination. Foraminiferal response to heavy metal pollution,
in particular, has been well documented with local extinctions resulting
in barren zones where contamination levels are high, and in transitional
to less polluted levels with assemblage modifications due to loss
of diversity, disturbance of live activities and test deformation
(double or enlarged apertures, twinning, protuberances, reduced
chamber size, or twisted chamber arrangements; Alve, 1995).
Evidence
suggests that Trochammina hadai Uchio, a foraminifer which
is abundant in many Japanese estuaries (Figure 7.1.; Matoba, 1970;
Matsushita and Kitazato, 1990; Uchio, 1962; and references therein),
is a particularly valuable pollution indicator in that country because
it dominates the foraminiferal assemblages in the most contaminated
brackish water locations (Kitazato, oral communication, 1998). For
example, core top sediment from Yokohama Port yielded 100% T.
hadai (Toyoda and Kitazato, 1995), and assemblages with >50%
T. hadai have been observed in the stressed environments
of Hamana Lake (Ikeya, 1977), Matsushima Bay (Matoba, 1970), and
Akkeshi Bay (Morishima and Chiji, 1951). Often these extreme abundances
are found near the heads of the bays, suggesting that high input
of anthropogenic organic matter may support these assemblages (Kitazato,
written communication, 1998).
We
first discovered T. hadai in the San Francisco Estuary in
1995 in sediment collected in 1993 near the San Francisco International
Airport and Marin Islands (McGann, 1995; McGann and Sloan, 1996).
Since then we have conducted a detailed investigation of past literature
and archived foraminiferal samples (Arnal et al., 1980; Locke, 1971;
Means, 1965; Quinterno, 1968; Slater, 1965), and have determined
that the species appears to have been introduced into the Estuary
between 1981 and 1983. The earliest sample in which T. hadai
has been found in the San Francisco Estuary is in one of four samples
collected in 1983 from the southern Bay, where it constituted 3%
of the foraminiferal fauna. By 19861987, T. hadai was
present at all 46 stations in the southern Bay, dominating the assemblage
with up to 89% of the foraminifers at these sites. The species was
also found in all of nine sediment samples collected from central
and southern Bay stations in 19901993, constituting up to
56% of the foraminifers.
Trochammina
hadai could have been transported to the Estuary in the sediment
associated with oysters used for commercial mariculture (Carlton,
1979), as ship hull fouling (WHOI, 1952), in anchor mud (Carlton
and Geller, 1993), in ballast water, or in sediment from ballast
tanks (Galil and Hülsmann, 1997). Yet, regardless of the mechanism
by which the species was introduced, environmental conditions within
the Estuary at the time of its arrival had to be conducive to the
species' growth and reproduction in order for it to not only survive,
but proliferate, as the evidence suggests. Japanese studies have
indicated that the environment preferred by T. hadai is a
very stressed one. Could the same be said for its new habitat in
the San Francisco Estuary?
Because
of the discovery of this invasive foraminiferal species in the Estuary,
we approached the San Francisco Estuary Institute to join their
Regional Monitoring Program with the intent to:
1.
Investigate the spatial and temporal distribution of all foraminiferal
species in the San Francisco Estuary. The last survey was completed
over 1.5 decades ago (19801981; Sloan, unpublished data).
2.
Monitor the present distribution and abundance of the invasive
Japanese species T. hadai.
3. Determine what effect the introduction of T. hadai has
had on the native foraminiferal assemblage in the San Francisco
Estuary.
4. Note any associations between sites where foraminifers indicative
of environmental stress, including specific species (e.g., T.
hadai) and morphological abnormalities, have been recovered
and the concentration of contaminants in the sediments at those
sites as determined by the Regional Monitoring Program.
In
this paper we report on the results of 2.5 years of bi-annual sampling
(August 19951997) of foraminifers in the San Francisco Estuary.
Methods
Bulk
sediment samples for microfaunal analysis were collected at 26 stations
during the wet (February) and dry seasons (August). Sediment was
obtained by subsampling the upper 2.5 cm of two successive van Veen
grabs. An effort was made to obtain approximately 200 cm3
of sediment at each site. In the laboratory, sediment samples were
wet-sieved through nested 0.063 mm, 0.150 mm, and 1.0 mm screens
to segregate the size fractions and remove the silt and clay-sized
particles. Sediment remaining on the screens was transferred to
filter paper and air-dried. Foraminifers were extracted exclusively
from the coarser fraction (> 0.150 mm) and the < 0.150 mm
fraction was archived. Analyzing only the larger size-fraction allows
for faunal comparison with previous provincial studies in the eastern
Pacific Ocean because most studies used this size fraction. Each
sample was split with the aid of a microsplitter into an aliquot
containing at least 300 benthic foraminifers, and all specimens
were picked and identified from this aliquot. If the sample contained
< 300 foraminifers, all that were present were picked. Sandy
samples containing few foraminifers were subjected to sodium polytungstate
floatation methods in order to concentrate the foraminifers before
picking. The slides and residues of this study are on file at the
U.S. Geological Survey in Menlo Park, California.
A cluster
analysis of the relationships between the foraminiferal assemblages
at the various sampling sites during the 2.5-year study was conducted
using Data Desk statistical software.
Results
Benthic
Foraminiferal Assemblages
A total
of 49 species of benthic foraminifers were recovered from the San
Francisco Estuary sediment samples collected from August 19951997.
Of these species, only five are common and five more are minor (Table
7.1). With the exception of H. germanica, these species are
common in estuaries along the Pacific seaboard of North America
(Murray, 1991) and have been used as ecological markers in sediments
dated ~125,000 years before present in San Francisco Bay (Sloan,
1980, 1992).
A Q-mode
cluster analysis of those samples with > 200 specimens grouped
them into three clusters and numerous outliers. The vast majority
of samples were joined into a single cluster. These samples are
characterized by a dominant T. hadai assemblage (> 50%),
with high abundances of A. beccarii and lower percentages of E.
excavatum. This foraminiferal assemblage occurs in the "core"
of the Estuary; that is, the center of San Pablo Bay, the central
Bay, and the southern Bay down to Redwood Creek. Here the salinity
ranges from approximately 2832 ppt.
The
second cluster grouped the Petaluma River samples and the August
1996 Pinole Point sample. These contain a foraminiferal fauna consisting
of dominant T. inflata and lesser abundances of A. beccarii and
T. hadai. Haynesina germanica and Elphidium spp. occur in
this fauna as well, but are generally less frequent.
The
last cluster joined the southern Bay stations of San Bruno Shoal
and the Dumbarton Bridge. The overlying water is less saline than
that to the north, and sediments obtained here include a varied
foraminiferal assemblage dominated by A. beccarii and E. excavatum,
lesser amounts of H. germanica and T. hadai, and rare T.
inflata.
The
stations in Suisun Bay and the extreme southern Bay were either
outliers or were not included in the cluster analysis because of
the low number of foraminifers obtained there. All of these stations
are characterized by overlying waters with very low salinity and
have similar foraminiferal faunas, with arenaceous species replacing
calcareous forms. The common estuarine foraminifers A. beccarii
and E. excavatum have been replaced by T. inflata, M. fusca, and
J. macrescens. In contrast, the Sacramento River, San Joaquin River,
and Guadalupe River stations contained no foraminifers, with the
water here considered to be too fresh to support these organisms
(Bradshaw, 1957, 1961).
Two
other stations present somewhat unique foraminiferal faunas: Richardson
and Horseshoe bays. The Richardson Bay sample from August 1995 is
characterized by an unusually high percentage of T. hadai
(86%) and T. inflata (12%), compared to the abundances of
these species for February 1996August 1997 (> 40% and >
5%, respectively). The lack of calcareous foraminiferal species
in this sample suggests that it has been subjected to conditions
conducive to dissolution. Further investigation of this sample is
warranted.
Horseshoe
Bay supports an unusual foraminiferal fauna for the San Francisco
Estuary because it contains typical coastal marine species such
as Bucella frigida (Cushman), Cibicides lobatulus (Walker and Jacob),
Nonionella stella Cushman and Moyer, Rosalina globularis d'Orbigny,
and Bulimina denudata Cushman and Parker, as well as abundant estuarine
species E. hannai, A. beccarii, T. hadai, and
E. excavatum. Such an "open ocean" fauna is not
surprising due to this station's proximity to the Pacific Ocean.
A preliminary
comparison of wet and dry season foraminiferal faunas at the 26
sites examined yielded variable results. Numbers of T. hadai
in samples collected in February 1996 along the shipping channel
through the northern Bay, San Pablo Bay, and the central Bay near
the Golden Gate are approximately half of the dry season values
for August 1995 and August 1996 (Sloan and McGann, 1996). These
abundances demonstrate the impact of decreased salinity, reflecting
high freshwater inflow. However, in the southern Bay, although salinity
decreased at all stations in February 1996, T. hadai abundances
at most stations increased slightly. Unfortunately, the foraminiferal
recovery in February 1997 was so poor at many of the stations that
a similar trend could not be discerned. Separate Q-mode cluster
analyses of August 1995February 1996 and August 1996February
1997 foraminiferal faunas were unable to discriminate between the
wet- and dry-season samples. These data suggest that although minor
fluctuations in species abundances exist, generally similar faunas
were found to occur at each site throughout the year.
Invasive
Foraminiferal Species Trochammina hadai
Trochammina
hadai has dominated 32% of the sites throughout the 2.5 years
of the RMP study (Figure 7.2a -
e). The species was found at 17 sites where it constituted up
to 93% of the foraminiferal fauna, but was not found at 7 locations
in the extreme northern and southern ends of the Bay. This investigation
has also found that the percent abundance of T. hadai in
the Estuary has remained stable, albeit remarkably high, throughout
the 2.5-year study period, and shows little, if any, seasonal alteration
at all but a few sites along the shipping channel.
The
species is abundant in RMP samples taken from the mud flats to a
depth of 13 m (SFEI, 1996, 1997). It is euryhaline, living at salinities
as low as 1215 ppt, but is more prevalent where salinities
range from 17.530 ppt. The species tolerates water temperatures
from 1119 °C, is more abundant on muddy rather than sandy
substrates, and thrives in the Estuary's year-round saturated oxygen
conditions. These environmental parameters are consistent with its
distribution in Japan's estuaries and harbors (Matoba, 1970; Matsushita
and Kitazato, 1990; Uchio, 1962).
While
this 2.5-year study of San Francisco Estuary foraminifers has proven
too short to determine what effect the introduction of T. hadai
has had on the native foraminiferal assemblage, a core recovered
from near San Francisco International Airport suggests that, at
least for this one location in the Estuary, a profound change in
the foraminferal population has occurred over the last 3,500 years
(McGann, 1995). Until the appearance of T. hadai, the foraminiferal
assemblage was dominated (5585%) by E. excavatum. With T.
hadai's arrival, E. excavatum dropped to 19% of the foraminifers
at 12.5 cm depth in the core, and has continued to decline
to an average of 5% in the southern Bay. Continued analysis of the
RMP's sediment samples and cores from other sources may allow us
to better understand the timing and geographic extent of this faunal
takeover.
Discussion
Pollution
Effect on the Foraminifers
Although
it must be noted that results of this phase of the study are only
preliminary, we have found no foraminiferal barren zones at stations
which have oceanographic conditions suggesting they should be present,
though many stations in the RMP are characterized as having high
concentrations of trace elements in the sediments (SFEI, 1997).
In addition, very few specimens exhibited the typical abnormal test
morphologies associated with contaminated environments. Instead,
only occasional deformed chambers were recovered; well within the
range considered normal for foraminiferal faunas (Alve, 1995).
The
only other type of foraminiferal test deformation seen, which may
be due to the presence of contaminants in the sediment, is a distinct
reddish-brown encrustation or precipitate on the tests of a few
specimens from Richardson Bay. This "growth" is similar
to that seen on specimens recovered in the vicinity of Hunter's
Point in San Francisco Bay, particularly in the region of the Navy
docks and nearby power plant (McGann et al., 1998). These areas
are considered to be among the most polluted in the Bay, especially
with regard to the heavy metals arsenic, chromium, cadmium, copper,
lead, nickel, zinc, and mercury. Benthic foraminifers recovered
from the Hunter's Point region in 1986 and again in 1997 exhibit
the encrustation. At a minimum, as with the Richardson Bay specimens,
affected specimens display the encrustation on the dorsal side,
usually at the proloculus, with one or more "iron-beads".
In extreme cases, such as those seen at Hunter's Point, dorsal and
ventral sides are heavily involved, resulting in all chambers being
obscured, although the area immediately surrounding the aperture
is never affected. This phenomenon may be due to the fact that the
streaming of pseudopodia in this area is sufficient to retard the
precipitate's growth (Kitazato, written communication, 1998) and
suggests that the encrustation is not a post-mortem effect. EDAX
and microprobe analyses of this encrustation demonstrates that it
is composed of iron, phosphorus, aluminum, magnesium, sodium, and
manganese.
The
encrustation occurs almost exclusively on the tests of the exotic
Japanese foraminifer Trochammina hadai. Of the two Hunter's
Point samples collected in 1986, T. hadai comprises 5966%
of the foraminiferal assemblages, with two-thirds to three-fourths
of these specimens displaying some evidence of the encrustation.
In the Richardson Bay RMP samples, only T. hadai specimens
are affected. The fact that nearly all of the affected foraminifers
are specimens of T. hadai suggests that the encrustation
is a chemical effect which occurs at or near the sediment surface,
as T. hadai lives with its dorsal side up and dominates the
foraminiferal assemblage in the uppermost 1 cm of sediment (Matsushita
and Kitazato, 1990), although it has also been observed living on
the sediment surface (Kitazato, written communication, 1998).
In
contrast to the association noted in Japan, our preliminary investigation
found no evidence of any relationship between the abundance of T.
hadai and the level of contaminants in the San Francisco Estuary,
except for the rare encrusted specimens recovered in Richardson
Bay. Further study in the Estuary may help clarify whether, in fact,
T. hadai can be considered a pollution-index species anywhere
else besides Japan.
Further
Work
The
RMP's foraminiferal study described in this report has, after only
2.5 years of monitoring, enhanced our knowledge of the basic distribution
of foraminifers within the San Francisco Estuary, and, specifically,
the dominance of the introduced Japanese species T. hadai.
Additional research is warranted to further characterize the temporal
and spatial patterns of foraminifers within the Estuary, particularly
since the conventional water characteristics (salinity, temperature,
etc.) and concentrations of contaminants vary from year to year.
We plan to expand the present data set by utilizing RMP archived
sediment samples to investigate foraminiferal assemblages in the
Estuary from the inception of the monitoring program to our initial
involvement. Archived material has already been obtained for March
1993February 1995. Among other things, we should be able to
determine if the depauperate calcium carbonate foraminiferal assemblage
noted in Richardson Bay in August 1995 is an anomalous occurrence,
and if the pattern of dominance by T. hadai in the Estuary
can be documented for a longer time period.
We
also feel the study should shift to an investigation of the distribution
of living foraminifera, enabling us to determine their absolute
abundances within the San Francisco Estuary and where the foraminiferal
species actually live, as opposed to where their tests are transported
after death. From these data we can gain insight into the seasonal
effects of river discharge and pollutants on the foraminiferal assemblages
and also possible food web alterations with the presence of the
organic matter-loving species T. hadai.
Acknowledgments
Bruce
Thompson's (San Francisco Estuary Institute) willingness to let
us participate in the Regional Monitoring Program is most gratefully
acknowledged. We would also like to thank the staff of Applied Marine
Sciences and Captain Gordon Smith of the University of California
at Santa Cruz for obtaining the foraminiferal samples used in this
study, and to our superb technical staff: Brad Carkin and Melanie
Moreno of the U.S. Geological Survey, and Elmira Wan and Jacquelin
Letran of the University of California at Berkeley. Many thanks
also to Charles Powell and Eileen Hemphill-Haley (U.S. Geological
Survey) and Kim Taylor (San Francisco Bay Regional Water Quality
Control Board) for reviews of the manuscript. This study was supported
by the San Francisco Bay Sediment Transport Study of the U.S. Geological
Survey.
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