Late 20th Century benthic foraminiferal distribution … · Late 20th Century benthic foraminiferal distribution in Central San Francisco Bay, California: Influence of the Trochammina

Late 20th Century benthic foraminiferal distribution inCentral San Francisco Bay, California: Influence of the

Trochammina hadai invasion

Mary McGannU.S. Geological Survey, Menlo Park, California, USA 94025

email: [email protected]

ABSTRACT: The distribution of foraminifera in most of San Francisco Bay is well documented, but this is not the case for thesubembayment known as Central Bay. To resolve this, 55 grab samples obtained in 1998 were analyzed to characterize the foraminiferalfauna in the surface sediments of the area. Thirty-five species were identified, including the invasive Japanese species Trochamminahadai that was introduced into the bay in the early 1980s. A cluster analysis of the samples from Central Bay produced three groups(biofacies) and one outlier. The Shallow Subtidal Biofacies is characterized by a marsh to shallow-subtidal agglutinated fauna, domi-nated by T. hadai but also including T. inflata, T. macrescens, Haplophragmoides subinvolutum, and Miliammina fusca. The Intermedi-ate Subtidal Biofacies, the Intermediate Subtidal Outlier, and the Deep Subtidal Biofacies are dominated by calcareous taxa, mostnotably Ammonia tepida, Elphidium excavatum, and Elphidiella hannai. Ammonia tepida is most abundant in the warmer, intermediatedepths of eastern Central Bay, abundances of E. excavatum peak in the cooler estuarine water near Alcatraz Island, and E. hannaithrives in the cold water west of Angel Island in a transitional setting between the deep subtidal estuarine and the nearshore marine envi-ronments. The recovery of oceanic species as far east as Angel Island indicate that western Central Bay is the most marine-influencedregion of San Francisco Bay.

Samples collected from 1965 onward were also compared with those from 1998 to investigate how the distribution of benthicforaminifera in Central Bay has changed over the latter half of the 20th Century, particularly in response to the invasion byTrochammina hadai. In 1998, T. hadai was recovered at 46 of 55 sites in Central Bay, comprising from 0.3 to 97% (mean = 23%) of theforaminiferal fauna. With the species’ affiliation for shallow environments, it is not unexpected that it dominated the fauna of the Shal-low Subtidal Biofacies (68-97%, mean = 77%) and was also a significant component of the Intermediate Subtidal Biofacies (7-51%, av-eraging 28%). In the deeper waters west of Alcatraz Island, the abundance of T. hadai was significantly less (mean = 8%), most likelyreflecting allochthonous specimens that were the result of post-mortem transport. A cluster analysis clearly distinguishes pre- andpost-invasion biofacies, illustrating how dominant T. hadai has become in Central Bay.

Keywords: benthic foraminifera, San Francisco Bay, Central Bay, invasive species, Trochammina hadai

INTRODUCTION

Although the distribution of foraminifera in surface sedimentsof San Francisco Bay is well known from the nearly 350 sitesinvestigated during the 1960s to early 1980s (Means 1965; Slat-er 1965; Quinterno 1968; Locke 1971; Connor 1975; Wagner1978; Arnal et al. 1980; Sloan, unpublished data from 1980–1981), only 20 of those sites were located in the subembaymentknown as Central Bay. As a result, the character of the foram-iniferal fauna in Central Bay remains the most poorly describedof any in San Francisco Bay. In addition, shortly after the com-pletion of these comprehensive distributional studies, a com-mon estuarine foraminifera in Japan, Trochammina hadaiUchio 1962, was introduced into the bay. The species mostlikely was transported to San Francisco Bay in ballast sediment,anchor mud, or sediments associated with oysters imported formariculture (McGann et al. 2000). Following the species’ ar-rival between 1981 and 1983, T. hadai proliferated, becomingone of the dominant foraminifera in the bay today. The goal ofthis present study is to investigate the distribution of both nativeand introduced foraminifera in Central Bay toward the close ofthe 20th Century.

SETTING

San Francisco Bay is the largest estuary on the west coast of theUnited States (Conomos et al. 1985), created from a structuraltrough that formed during the early Pleistocene when the ances-tral San Joaquin and Sacramento Rivers, and Coyote Creekformed a drainage basin parallel to a coastline west of the pres-ent Golden Gate Bridge (Lawson 1894; 1914; Atwater et al.1977; Atwater 1979) that was later inundated at least four timesby seawater during Pleistocene and Holocene interglacials(Gilbert 1917; Louderback 1941; 1951; Sloan 1992; McGann etal. 2002). Today, San Francisco Bay consists of three sub-embayments (text-fig. 1): North Bay (including San Pablo andSuisun Bays as well as the shallow embayments of Grizzly andHonker Bays), Central Bay (including Richardson Bay), andSouth Bay (Chin et al. 2004).

Central Bay is defined here to encompass the open water andintertidal margins (i.e., mudflats and marshes) from Point SanPablo and Point San Pedro to the north, the Golden Gate Bridgeto the west, the shores of Richmond and Berkeley to the east,and the San Francisco-Oakland Bay Bridge to the south

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(text-fig. 2). It has the largest water volume of the threesubembayments (The Bay Institute 1998; Chin et al. 2004). De-spite this fact, Central Bay averages a depth of only 11m, frommean lower low water (MLLW; the average height of the lowerof the two daily low tides) depth, which renders submergedrock knobs (Anita, Blossom, Harding, Shag, and Arch Rocks) apotential hazard to the shipping industry (Chin et al. 2004). Incontrast, the deepest part of San Francisco Bay is in westernCentral Bay, where depths near the Golden Gate Bridge reach amaximum of 113m (Hanes and Barnard 2007).

One of the strongest tidal flows in the world passes through theGolden Gate. Currents exceed 2.5 m/s with an enormous tidalprism of 2 x 109 m3, resulting in about 500 billion gallons of wa-ter moving though the narrow opening every six hours (SanFrancisco Chronicle 2006; Hanes and Barnard 2007; Barnard etal. 2008). As a result, sediment is constantly moving in and outof San Francisco Bay, forming large sand waves on the floor ofCentral Bay and seaward of the Golden Gate (Chin et al. 2004;Hanes and Barnard 2007). Because of this dynamic environ-ment, western Central Bay is deep and characterized by thepresence of very coarse substrate as finer sediments are win-nowed (Rubin and McCulloch 1979; text-fig. 3). At times, sedi-ment-laden currents also flow between Central Bay and bothNorth and South Bays (see Fig. 2 of McGann et al. 2013), asshown by the coarse sand north of Angel Island and very coarsesand in the vicinity of Treasure Island (text-fig. 3). Surprisingly,the latter was not evident in 2010 (text-fig. 4; McGann et al.2013). With each tidal cycle there is also a slack tide when thecurrents are weak and sediment may be deposited.

Eastern Central Bay differs from the western portion in that it isshallow, subjected to less marine-exchange, and dominated byfine-grained sediment that is prone to wind-generated currentsinstead of strong tidal scouring (San Francisco Estuary Institute1997; 2000; LTMS 1998; McGann et al. 2013). Samples from1998 (text-fig. 3), supplemented with some collected in 2010(text-fig. 4), show that clay and silt are present to the easternshoreline of Central Bay.

Central Bay is the most marine-influenced region of San Fran-cisco Bay because it connects with the Pacific Ocean throughthe Golden Gate (LTMS 1998; San Francisco Estuary Institute2000). During the late 1990s, salinity in this subembaymentranged between ~26 and 30 in the summer (text-fig. 5), whereasthe winter influx of freshwater from the Sacramento-SanJoaquin Delta and local watersheds decreased salinity to~14–24, and even as low as 4 in the eastern portion of CentralBay (San Francisco Estuary Institute 1997; 1999; 2000). Simi-larly, bottom water temperatures at this time fluctuated substan-tially between seasons, from ~15–19°C in summer to ~10–12°Cin winter, but occasionally as warm as 14–15°C (text-fig. 6).These compare to the fairly constant values of ~13–14°C in themarine realm off San Francisco Bay (Mendelssohn andSchwing 2002).

PREVIOUS WORK

Several scientific cruises in the late 19th and early 20th centu-ries investigated the distribution of marine organisms (includ-ing foraminifera) in the Pacific Ocean. Among these were thevoyages of the H.M.S. Challenger from 1873-76 (Brady 1884),the U.S.S. Albatross from 1888–1911 (Flint 1899; Bagg 1908;Cushman 1910; 1911; 1913; 1914; 1915; 1917), and the U.S.S.Nero from 1899–1900 (Flint 1905). Their sampling programs,

however, focused on the deeper waters and excluded the Cali-fornia coast. The fact that no collections were made within thebay or on its adjacent coastline in those early years (Hanna andChurch 1927) is somewhat surprising because San FranciscoBay was the homeport of the U.S.S. Albatross for many years. Itwas not until 1912–1913, after the U.S.S. Albatross was foundto be unseaworthy, that she explored San Francisco Bay, acquir-ing 43 dredge samples from South Bay to Carquinez Strait(Packard 1918b). That endeavor produced publications on thesedimentology and overlying oceanographic parameters (Sum-ner et al. 1914) and the distribution of mollusks (Packard 1918a;1918b), but the foraminifera were never studied.

The earliest published study of foraminifera in the vicinity ofSan Francisco Bay was that of Hanna and Church (1927), whoreported on a single sediment sample collected for the SteinhartAquarium in January 1926 in the open ocean between PointReyes and the Farallon Islands from a depth of about137–155m. They documented 37 species, including several re-ported for the first time from the continental shelf and adjacentslope off California. Shortly thereafter, McDonald and Diediker(1930) reported the distribution of foraminifera at 19 locationsin San Francisco Bay from South Bay to Suisun Bay, seven ofwhich were in Central Bay (text-fig. 2). They included two ad-ditional sites outside the Golden Gate at Seal Rock and in HalfMoon Bay. Unfortunately, they did not state when or by whatmeans they acquired their samples. The authors identified eightspecies of foraminifera within the bay and 13 outside the bay,with living specimens recovered at nearly every station. Theyconcluded that the higher species diversity outside the bay re-flected more favorable conditions for foraminifera, bottom con-ditions within the bay did not seem to have an influence on “thelife of the forms,” and Bulls Head Point (western Suisun Baynear Martinez) roughly defined the limit of foraminiferal occur-rence in San Francisco Bay. McDonald and Diediker (1930)also noted a possible relationship between environmental fac-tors (salinity and temperature) and the distribution of the mostabundant species.

It was not until the 1960s that the distribution of foraminifera insurface sediments in San Francisco Bay was investigated in de-tail. Among the studies were those of Slater (1965) in SuisunBay, Locke (1971) in San Pablo Bay, Means (1965) and Connor(1975) in Richardson Bay, and Quinterno (1968) and Arnal etal. (1980) in South Bay. In addition, Wagner (1978) and Sloan(unpublished data from 1980-1981) undertook bay-wide stud-ies. Published foraminiferal data applicable to the present studyin Central Bay include those of Locke (1971) for nine sites fromPoint San Pablo to the Richmond-San Rafael Bridge, Means(1965) for 34 sites in Richardson Bay, Raccoon Strait, andnorthwestern Central Bay, and Sloan (unpublished data) forthree sites sampled in August 1980 and February 1981 from theshallow waters near the Berkeley Pier on the eastern side ofCentral Bay (text-fig. 2). Wagner (1978) also obtained threegrab samples between the Tiburon Peninsula and Point Rich-mond, and three more from the deep waters between AlcatrazIsland and the Golden Gate, but only provided faunal counts forthe latter. All of these investigations occurred before the intro-duction of Trochammina hadai.

In 1997, SFEI (San Francisco Estuary Institute) obtained grabsamples from 23 sites throughout San Francisco Bay in order tocharacterize the distribution of foraminifera after the introduc-tion of Trochammina hadai (McGann and Sloan 1999). Five of

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Mary McGann: Late 20th Century benthic foraminiferal distribution in San Francisco Bay: Influence of the Trochammina hadai invasion

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Micropaleontology, vol. 60, no. 6, 2014

TEXT-FIGURE 1

Location map of San Francisco Bay, including the three subembayments: North Bay (including San Pablo, Suisun, Grizzly, and Honker Bays), CentralBay (including Richardson Bay), and South Bay.

the sites are located within Central Bay: Horseshoe Bay, Rich-ardson Bay, Red Rock, Point Isabel, and Yerba Buena Island(text-fig. 2).

METHODS

In early 1998, the USGS (U.S. Geological Survey) collectedsamples from Central Bay to determine the nature and thickness

of its Quaternary sediment. In conjunction with a multibeamsurvey conducted in 1997, new multibeam and sidescan sonardata was collected onboard the RV David Johnston (USGSCMG cruise J-1-98-SF) from January 8–23 to investigate thesurficial and shallow subsurface deposits of the bay. In addition,56 samples were obtained by a small Van Veen grab sampler tocharacterize the texture of surface sediments for benthic habitatidentification, sediment distribution, and transport studies inCentral Bay (text-fig. 2).

In 2003, Watt performed a grain-size analysis of subsamplesfrom 55 of the 56 sediment grab samples obtained in the field in1998; sample 9 could not be located. Sediment was separated bywet-sieving and then analyzed at half phi intervals from -1 phito 11 phi and at 14 phi using a Beckman Coulter Light Scatter-ing (LS) particle analyzer. Individual grain size distributionswere calculated using SedSize, a UNIX-based computer soft-ware program developed by the USGS.

In 2008, sediment from the other subsamples of all but one(missing sample 9) of the 56 samples were analyzed forforaminifera (this study; Table 1). It is unfortunate that thesesamples were collected a decade earlier because it was no lon-ger possible for histologic staining to distinguish those speci-mens that were alive at the time of collection (Bernhard 1988;2000). The sediment samples were wet-sieved through nested63µm, 150µm and 1.0mm screens to remove clay (<63µm) andseparate size fractions. The residue was then transferred to filterpaper and air-dried.

Heavy liquid floatation with sodium polytungstate isolatedforaminifera from the <1.0mm size fraction. The floated resi-dues were then split with the aid of a microsplitter into analiquot containing at least 300 benthic foraminifera and all spec-imens were picked and placed on 60-grid micropaleontologicalslides. If the sample contained <300 foraminifera, all that werepresent were picked. The specimens were then sorted by speciesand adhered to the slides. Both slides and residues are on file atthe USGS in Menlo Park, California.

Due to the small number of foraminifera recovered from manyof the samples, relative foraminiferal species abundances werecomputed using a sum of benthic foraminifera in the 40 samplesthat yielded at least 50 specimens. Once converted to frequencydata, a Q-mode cluster analysis was utilized to describe the rela-tionship between the benthic foraminiferal faunas. Cluster anal-ysis, which groups the samples according to their degree ofsimilarity, was based on a square root transformation of thedata, a Bray-Curtis similarity coefficient, and amalgamated by agroup-averaged linkage strategy. These methods treat all spe-cies equally while providing the most realistic grouping of thesamples (Clarke and Gorley 2006). Primer v. 6, a statistical soft-ware package created by Primer-E, Ltd., was used for this anal-ysis (Clarke and Gorley 2006).

RESULTS

The Central Bay samples yielded 35 species of agglutinated andcalcareous benthic foraminifera (Table 2), with species richnessranging from 3-20 (mean = 9). All of the species are found to-day inhabiting nearshore, shallow embayments or estuariesalong the Pacific Coast of North America (Phleger 1967; Scottet al. 1976; Ingle 1980; Murray 1991; Jennings and Nelson1992; McCormick et al. 1994; McGann 2007). Included amongthem is the invasive species Trochammina hadai, which has

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TABLE 1

Sample number, water depth (m), and location (latitude and longitude)of the sampling sites of the 1998 Central Bay study (USGS cruiseJ-1-98-SF).

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TEXT-FIGURE 2

Location of the foraminiferal study sites in Central Bay. Sites includes those collected in 1998 (this study), as well as those of McDonald and Diediker(1930), Means (1965), Locke (1971), Wagner (1978), Sloan (1980-1981, unpublished data), and SFEI (McGann and Sloan 1999). The site locations ofMcDonald and Diediker are approximated from the original source. Bathymetric contours in meters. YBI = Yerba Buena Island.

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TEXT-FIGURE 3

Interpolated mean grain size of surface sediment samples collected in 1998 (this study) in Central Bay.

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TEXT-FIGURE 4

Interpolated mean grain size of surface sediment samples collected in 2010 in Central Bay.

now been found in 14 ports and estuaries from San Diego Bay,southern California to Prince William Sound, Alaska (McGannet al. 2000; McGann, unpublished data). Of the species recov-ered in Central Bay, the most common are Ammonia tepida(Cushman 1926), Elphidiella hannai (Cushman and Grant1927), Elphidium excavatum (Terquem 1875), T. hadai, andTrochammina inflata (Montagu 1808) (Table 3). In the 1998survey, T. hadai was present throughout much of Central Bay,occurring at 46 of 55 sites (text-fig. 7). The species accountedfor >50% of the foraminiferal fauna at several sites, and a maxi-mum of 97% at one locality.

It should be noted that presently, Ammonia tepida is a taxo-nomic problem. The species is one of two or three in the generaAmmonia recognized in brackish waters of bays, estuaries andlagoons worldwide, that are now thought to include possibly>25–30 molecular types instead (Hayward et al. 2004). In thepresent study, the taxonomic designation A. tepida will con-tinue to be used until further molecular information suggestsotherwise, since specimens living in San Francisco Bay havenot yet been sequenced (Hayward et al. 2004), the morphotypebest resembles Ammonia tepida based on specific morphologi-cal characters, (i.e., number, size, and thickness of chambers,and presence or absence of limbate sutures, sutural ornamenta-tion, and umbilical fillings of various sizes), and previous stud-ies in the bay have identified the species by this name (e.g.,Means 1965; Slater 1965; Quinterno, 1968; Arnal et al. 1980).

Q-mode cluster analysis of the 1998 Central Bay foraminiferaldata grouped the samples into three clusters and one outlier(text-fig. 8). They are referred to here as the Shallow Subtidal,Intermediate Subtidal, and Deep Subtidal Biofacies, and the In-termediate Subtidal outlier.

Foraminifera from eight samples recovered at water depths of6-14m (mean = 9m; Table 4) grouped to form the ShallowSubtidal Biofacies (text-fig. 8). These sites are located in themiddle of Central Bay from the Richmond-San Rafael Bridge tothe western end of the Berkeley Pier (text-fig. 9). The fauna ofthis assemblage is characterized by low species richness (mean= 6 species/sample), rare calcareous species (accounting for<2% of the assemblage on average), and an abundance of ag-glutinated species. Trochammina hadai averages 77% and dom-inates this assemblage, Trochammina inflata is common (17%),and Ammobaculites exiguus Cushman and Brönnimann 1948,Haplophragmoides subinvolutum Cushman and McCulloch1939, Miliammina fusca (Brady 1870), and Trochamminamacrescens Brady 1870 are present in lower numbers. Sedi-ment grain size ranges from fine to coarse silt averaging 5.59phi, or medium silt (Table 5).

Cluster analysis strongly separated samples assigned to theShallow Subtidal Biofacies from all other samples (text-fig. 8).Whereas the fauna of this assemblage is dominated by aggluti-nated taxa, those of the two remaining biofacies and the outlierare dominated by calcareous species.

Like the Shallow Subtidal Biofacies, the Intermediate SubtidalBiofacies is a grouping of eight samples (text-fig. 8). Thesesamples are located along a crescent from the eastern side of theTiburon Peninsula and Angel Island south to near Fort Mason,with one additional sample on the eastern side of Treasure Is-land (text-fig. 9). The samples range in depth from 13–35m(mean = 18m) and are composed of fine silt to coarse sand withshells, averaging 4.77 phi, or coarse silt (Table 5). Species rich-

ness of this assemblage is 11. Although Trochammina hadaicontinues to be a significant constituent of this assemblage (av-eraging 28%), Ammonia tepida is slightly more abundant(30%); Elphidium excavatum (14%) and Elphidiella hannai(14%) are common.

The Intermediate Subtidal Outlier is sample 53, a very fine sand(3.20 phi units; Table 5) collected south of the Richmond-SanRafael Bridge in the vicinity of Red Rock (text-fig. 9). Thedendrogram (text-fig. 8) shows that this sample has characteris-tics of both the Shallow Subtidal and Intermediate SubtidalBiofacies, although it is more closely allied with the latter. The16m water depth at which the sample was obtained is greaterthan that of the average depth (9m) of the Shallow SubtidalBiofacies, and less than the average depth (18m) of the Interme-diate Subtidal Biofacies. In addition, its species richness valueof 9 is between the 6 and 11 of those other biofacies, respec-tively. This outlier sample yielded abundant Ammonia tepida(40%) and Trochammina inflata (21%), common Elphidiellahannai (16%), and less frequent Elphidium excavatum (9%),Buliminella elegantissima (d’Orbigny 1839) (4%), andHaplophragmoides subinvolutum (4%).

The Deep Subtidal Biofacies is represented by the highest num-ber of samples, comprising 23 (text-fig. 8). With the exceptionsof sample 40 from just east of Angel Island, and sample 46 fromthe Tiburon Peninsula, all are were collected in the western por-tion of Central Bay from Angel Island to the Golden GateBridge (text-fig. 9). These samples were obtained from depthsof 14–60m, (mean = 25m). They range from coarse silt to verycoarse sand with an average of 1.40 phi units, or medium sand(Table 5). Abundant species in this assemblage are Elphidiellahannai (mean = 43%; max. = 78%) and Ammonia tepida (mean= 24%). Common species include Elphidium excavatum (12%)and Trochammina hadai (8%). Numerous nearshore marinespecies are also present, including Buccella tenerrima (Bandy1950), Cassidulina limbata Cushman and Hughes 1925,Cassidulina tortuosa Cushman and Hughes 1925, Eggerellaadvena (Cushman 1922), Lagena pliocenica Cushman and Gray1946, L. striata (d’Orbigny 1839), Nonionella basispinata(Cushman and Moyer 1930), N. stella Cushman and Moyer1930, Eponides cribrorepandus (Asano and Uchio 1951),Rosalina globularis d’Orbigny 1826, Rotorbinella campanu-lata (Galloway and Wissler 1927), R. turbinata (Cushman andValentine 1930), and Trichohyalus ornatissima (Cushman1925). The Deep Subtidal Biofacies has a relatively high spe-cies richness of 12 due to its inclusion of these marine taxa.

Fifteen samples were excluded from the cluster analysis be-cause they yielded fewer than 50 specimens (Table 2). Three ofthese samples are very fine- to fine-silt, while the rest are amongthe most coarse-grained sediment encountered in this study,ranging from medium to very coarse sand with shells (averaging0.65 phi units; Table 5). They are characterized by an extremelylow average benthic foraminiferal number (specimens/gram drysediment ) of 0.1, and low average faunal richness of 5.

DISCUSSION

Distribution of Foraminifera

Wide fluctuations in water temperature and salinity, as well asacidic environmental conditions due to high organic input, aretypical of marshes and very shallow subtidal estuaries. Theseconditions are stressful to most species of foraminifera; hence

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TEXT-FIGURE 5

Interpolated bottom water salinity (psu) for Central Bay based on the SFEI samples collected between August 1995 and February 1998.

these marginal environments are often characterized by lowspecies diversity (Murray 1973) and species richness (Phleger1970). Dissolution of calcite results in the dissolution of calcar-eous tests, so they are often poorly or not preserved and aggluti-nated taxa predominate (Parker and Athern 1959; Arnal 1961;Phleger 1967; Scott and Medioli 1980; Scott and Leckie 1990;Jennings and Nelson 1992). Similar faunal characteristics de-fine the Shallow Subtidal Biofacies, which has low species rich-ness (mean = 6) and domination by agglutinated species,primarily Trochammina hadai (77%), but also others indicativeof marshes (Ammobaculites exiguus, Haplophragmoides sub-involutum, Miliammina fusca, and Trochammina macrescens).This assemblage was recovered in the shallow regions of Cen-tral Bay (mean depth = 9m), which has the lowest average cur-rent velocity of all of Central Bay for the entire tidal cycle(McGann et al. 2013) as well as the finest sediment, being fineto coarse silt (text-fig. 3; Table 5). Because a similar aggluti-nated-dominated fauna is present in the marshes of Richmond(text-fig. 2; Weber and Casazza 2006), it is assumed the Shal-low Subtidal Biofacies extends to the eastern margin of CentralBay.

Associated with increasing water depth (13–35m) in CentralBay is an increase in average current velocity, particularly atpeak ebb and flood tides (McGann et al. 2013), and an increasein grain size from fine silt to coarse sand (text-fig. 3). The Inter-mediate Subtidal Biofacies occurs here and is distinguished byits higher species richness of 11 and dominance by calcareousspecies (primarily Ammonia tepida, Elphidium excavatum, andElphidiella hannai, although Trochammina hadai still com-prises more than a quarter of the fauna), which reflects the deep-ening water and more stable environmental conditions.Ammonia tepida, or at least specimens with a similar morphol-ogy since the taxonomy is questionable (Hayward et al. 2004),have been reported living on or in the sedimentary substrate(Debenay et al. 1998) of shallow, brackish to hypersaline envi-ronments, preferring regions with salinities <33 (Debenay et al.1998) and an optimum range of 20–40 (Bradshaw 1957). Thespecies also thrives in warm temperate to tropical regions, ide-ally with temperatures between 24°C and 30°C (Bradshaw1957). For this reason, A. tepida is not found in the cooler wa-ters of the eastern Pacific north of about Samish Bay, Washing-ton (Scott 1974; Jones and Ross 1979). Elphidium excavatumalso lives in wide-ranging salinity regimes (11–35), but preferscolder water temperatures than A. tepida (0–12°C; tolerates upto 22°C) (Brodniewicz 1965; Murray 1965; 1970; Haake 1967).And like E. excavatum, E. hannai prefers cold water, living inestuaries and on the inner shelf as far north as Cordova, Alaska(Cushman and McCulloch 1940; Echols and Armentrout 1980;Murray 1991; and as Elphidiella nitida Cushman 1941 inCockbain 1963 and Bergen and O’Neil 1979). Abundant A.tepida in the Intermediate Subtidal Biofacies indicates this as-semblage prefers warmer water and somewhat shallow condi-tions, typical of faunas in other locations in San Francisco Bay(i.e., San Pablo and Richardson Bays as well as South Bay;Means 1965; Slater 1965; Quinterno 1968; Locke 1971; Arnalet al. 1980; McGann and Sloan 1999; McGann et al. 2013).

Three samples (15, 16, and 17a) from the Intermediate SubtidalBiofacies were obtained from the Alcatraz dredge disposal sitesouthwest of Alcatraz Island (text-fig. 9). Although first used in1894 (LTMS 1994), the area was formally designated a disposalsite in 1972 (LTMS 1998) and was heavily used until 1987. Atthat time, the mound had become high enough that it was

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TABLE 2

Benthic foraminifera identified in the 1998 Central Bay samples (inbold) with species and synonomies used in the studies of McDonald andDiediker (1930), Means (1965), Locke (1971), Wagner (1978), Sloan(1980-1981, unpublished data), and SFEI (McGann and Sloan 1999).

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TEXT-FIGURE 6

Interpolated bottom water temperature (°C) for Central Bay based on the SFEI samples collected between August 1995 and February 1998.

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TEXT-FIGURE 7

Abundance (in percent frequency) of the invasive species Trochammina hadai in the 1998 Central Bay foraminiferal samples.

thought to be a possible hazard to navigation. A subsequent pol-icy change not only significantly reduced the amount and fre-quency of sediment being disposed of there, but placedlimitations on the sediment contaminant load allowed as well(LTMS 1995; Chin et al. 2004). The native material at the site ispredominately fine to coarse sand with occasional finer silt andnearby are areas of bedrock and boulders (LTMS 1998). In con-trast, the dredged material dumped in the area is mostlyfine-grained (clays and silts) with elevated levels of pollutantsfrom urbanization, including heavy metals, oil, grease, TRPHs,and PAHs (LTMS 1998). Only sample 17a contains abundantHaynesina germanica (Ehrenberg 1840) (18.3%), a specieswhich prefers organic matter (Arnal et al. 1980; Frontalini et al.2013; Melis and Covelli 2013) and is tolerant of pollutants(Armynot du Châtelet et al. 2004; Carboni et al. 2009), the pres-ence of both of which are often associated with finer-grainedsediment. Yet, sample 17a is more coarse (2.57 phi units; finesand) than samples 15 and 16 (6.05-6.26 phi units; fine silt; Ta-ble 5). Also of interest is the absence of Eggerella advena inthese three samples although it is recovered occasionally else-where in Central Bay. The species is another organic matter-fa-voring taxon that is common to polluted coastal waste dischargeregions (Watkins 1961; Bandy et al. 1965; Clark 1971; Schaferand Cole 1974; Schafer and Young 1977; Bates and Spencer1979; McGann et al. 2003) and a pioneer colonizer in formerpolluted areas (Schafer 1982).

Sample 53 is the Intermediate Subtidal Outlier and is the onlyone of two samples (the other being sample 30) used in the clus-ter analysis that did not contain any specimens of the invasiveTrochammina hadai. Although it has abundant faunal elementsof both the Shallow Subtidal Biofacies (Trochammina inflata)and Intermediate Subtidal Biofacies (Ammonia tepida), thefauna of the Intermediate Subtidal Outlier is dominated by A.tepida (40%) and indicates warmer, relatively shallow, subtidalestuarine conditions.

The deepest samples collected in this study, ranging from14-60m, are coarse silt to very coarse sand (Table 5), reflectingextremely high average current velocity for nearly all of thetidal cycle with the exception of the slack tide (McGann et al.2013). The Deep Subtidal Biofacies collected here, with domi-nant Elphidiella hannai (mean = 43%; max. of 78%), commonAmmonia tepida, and a variety of nearshore marine species(Lankford and Phleger 1973; McGann 2007) represents acool-water, transitional fauna between those of the deepsubtidal estuarine and the nearshore marine environments. Sim-ilarly, Arnal et al. (1980) considered the presence of E. hannaiindicative of marine water, finding the species most abundant inthe coarse sediment associated with the deep channel (12–22m)of South Bay and leading them to suggest that oceanic waterwas present in this channel for most of the year.

Fifteen samples were excluded from the cluster analysis be-cause they had so few foraminifera; with few exceptions, theywere the coarsest samples recovered in this study. The ex-tremely low average benthic foraminiferal number of 0.1 andlow average species richness of 5 characteristic of these 15samples reflects how difficult it is for most benthic foraminiferato colonize extremely high-energy environments (Murray1991).

Faunal changes influenced by the introduced foraminiferaTrochammina hadai

The invasive foraminifera Trochammina hadai is thought tohave been introduced into San Francisco Bay in the early 1980s,as there is no evidence of the species in samples collected fromthe bay before 1983 (McGann et al. 2000; McGann 2014). Fif-teen years later, T. hadai had spread throughout the estuary,from the eastern edge of San Pablo Bay in North Bay to the ex-treme southern limit of South Bay (McGann and Sloan 1999;McGann 2014). In Japan and elsewhere along the eastern Pa-cific seaboard, the species thrives in shallow estuarine waters(McGann et al. 2000). Similarly, T. hadai was abundant in the

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TEXT-FIGURE 8Dendogram of the Q-mode cluster analysis of the 1998 Central Bay sam-ples based on the quantitative foraminiferal abundances (in percent fre-quency). Three biofacies and one outlier are recognized.

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TEXT-FIGURE 9

Spatial distribution of the 1998 Central Bay foraminiferal biofacies identified by the Q-mode cluster analysis. Bathymetric contours in meters. YBI =Yerba Buena Island.

shallow eastern and northern portions of Central Bay in 1998,often accounting for more than 50% of the fauna, and a maxi-mum of 97% at site 35 near the end of the Berkeley Pier(text-fig. 7; Table 3) and 91% at the nearby SFEI site of PointIsabel (McGann et al. 2013). In contrast, the abundance of T.hadai was significantly less in the deeper waters west ofAlcatraz Island, averaging only 8% of the assemblage. It is as-sumed that the specimens recovered at these deep stations wereallochthonous and had been subjected to post-mortem transport,although the 1998 samples were not stained to confirm this.

With Trochammina hadai’s affinity for shallower environments,it is not surprising that it dominated the fauna of the ShallowSubtidal Biofacies (68-97%, mean = 77%; Table 4), and was ameaningful element of the Intermediate Subtidal Biofacies aswell (7–51%, averaging 28%). In the deep subtidal estuarine tonearshore marine environment characterizing western CentralBay, the species was a minor element in the foraminiferal fauna(i.e., the Deep Subtidal Biofacies), reflecting its possible trans-port to the area.

533


TEXT-FIGURE 10Dendogram of the Q-mode cluster analysis of the 1965 to 1998 Central Bay samples based on the quantitative foraminiferal abundances (in percent fre-quency). Sites includes those collected in 1998 (this study), as well as those of Means (M-; 1965), Locke (L-; 1971), Wagner (W-; 1978), Sloan (S-;1980-1981, unpublished data), and SFEI (SFEI-; McGann and Sloan 1999). Seven biofacies and one outlier are recognized.

Comparison to previous studies

It is of interest to investigate to what extent the distribution ofbenthic foraminifera in Central Bay has changed over the 20thCentury. This can be accomplished by comparing the distribu-tional patterns in Central Bay from 1930 to 1998 as reported byMcDonald and Diediker (1930), Means (1965), Locke (1971),Wagner (1978), Sloan (1980–1981, unpublished data), andSFEI (McGann and Sloan 1999), as well as that revealed fromthe present study’s analysis of the 40 samples collected in 1998.

Of the 19 locations McDonald and Diediker (1930) studied,seven are located within Central Bay. Among these areManzanita (Marin City), Tiburon Point, Crab Cove (CorteMadera), San Quentin Point, Point San Pablo, and two sites at

Fort Point off San Francisco (text-fig. 2). They identified thespecies obtained at each site (Table 6), but did not publish quan-titative data. Their fauna includes three species that are commonin Central Bay today: Ammonia tepida was found at all sites ex-cept one of those at Fort Point, while both Elphidiella hannaiand Elphidium sp. were recorded at four sites. Additionally,Cibicides sp., Discorbis monicana Zalesny 1959 (identified asRotalia rosacea d’Orbigny 1826), Trochammina sp., and aquestionable occurrence of Quinqueloculina sp. were each re-stricted to only one or two of the seven sites. Better comparisonscan be made using the percentage abundances of the benthicforaminiferal species provided by Means (1965), Locke (1971),Wagner (1978), Sloan (1980-1981, unpublished data), and SFEI(McGann and Sloan 1999) .

534


TABLE 3

Species abundances of the benthic foraminifera in the 1998 Central Bay samples, given as a percentage of total foraminifera/sample.

535


TEXT-FIGURE 11Spatial distribution of the 1965 to 1998 Central Bay foraminiferal biofacies identified by the Q-mode cluster analysis. Bathymetric contours in meters.YBI = Yerba Buena Island.

Cluster analysis separated the 1965-1998 samples into sevengroups and one outlier based on the presence/absence of the in-vasive foraminifer Trochammina hadai, as well as distinctbiofacies associated with depth (text-fig. 10). Samples collectedin 1997 (SFEI) and all but one in 1998 (from site 53) togetherformed three groups (text-fig. 10) similar to the clustering ofonly the 1998 samples (text-fig. 8). All of these samples con-tained T. hadai: thus, their groupings are referred to as either thePost-Invasion Shallow Subtidal Biofacies, Post-Invasion Inter-mediate Subtidal Biofacies, or Post-Invasion Deep SubtidalBiofacies. These biofacies are so similar to the ShallowSubtidal, Intermediate Subtidal, and Deep Subtidal Biofacies ofthe 1998 data set discussed above in detail that no further expla-nation is needed here (see text-fig. 11 for locations).

Four distinct clusters represent all of the samples collected be-tween 1965 and 1981, and sample 53 of the present study(text-fig. 10). None of these samples yielded Trochamminahadai; hence, these clusters are labeled as the Pre-InvasionIntertidal Biofacies, Pre-Invasion Shallow Subtidal Biofacies,Pre-Invasion Intermediate Subtidal Biofacies, and Pre-InvasionDeep Subtidal Biofacies. In addition, there is the Pre-InvasionIntertidal Outlier.

Three samples obtained from an average depth of 1.3m form thePre-Invasion Intertidal Biofacies (text-fig.10). Two are fromRichardson Bay and the third is from just off the Tiburon Penin-sula near Raccoon Strait (text-fig. 11). The Pre-InvasionIntertidal Biofacies is dominated by agglutinated species com-mon to tidal marshes and intertidal zones of bays and lagoons,and includes Ammobaculites exiguus, Miliammina fusca,Textularia earlandi Parker 1952, Trochammina inflata, T.kelletae Thalmann 1932, T. macrescens, and T. pacificaCushman 1925 (Phleger 1967; Scott et al. 1976; Jennings andNelson 1992; McGann 2007).

The Pre-Invasion Intertidal Outlier (M-38; text-fig. 10) was col-lected at 0.5m depth in the extreme northwest corner of Rich-ardson Bay (text-fig. 11) and has a composition similar to thesamples of the Pre-Invasion Intertidal Biofacies but with higherdominance by Miliammina fusca, T. inflata, and T. macrescens.The unique faunal character of this sample is due to its proxim-ity to a freshwater creek flowing into Richardson Bay (Means1965).

Of the pre-invasion biofacies, the largest clustering of samplesincludes eight of Locke’s (1971) samples from Point San Pablo

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TABLE 4

1998 Central Bay foraminiferal biofacies, number of samples in the biofacies, depth range and average depth (in meters), representative species, percent-age abundance range and average percentage abundance, and ecological interpretation.

to the Richmond-San Rafael Bridge, 13 of Means’ (1965) fromRichardson Bay, two samples from one of Sloan’s (1980-1981)sites in shallow waters south of the Berkeley Pier, and sample53 of the current study (text-figs. 10, 11). These samples clus-tered as the Pre-Invasion Shallow Subtidal Biofacies. This as-semblage is from an average depth of 4.3m and consists of bothagglutinated and calcareous species, suggesting it is transitionalwith characteristics of both intertidal and deeper subtidal

biofacies. As such, it is similar to the Post-Invasion ShallowSubtidal Biofacies.

The Pre-Invasion Intermediate Subtidal Biofacies (text-fig. 10)consists of 17 samples, most of which were collected whereRichardson Bay meets Central Bay (Means 1965), and threesamples from two sites near the Berkeley Pier (Sloan1980–1981) (text-fig. 11). The water depth of this assemblage

537


TABLE 5

Water depth (m), sample weight, total foraminifera counted, benthic foraminiferal number, species richness, biofacies, sediment grain size and sedimentsize class of the 1998 Central Bay samples. Sediment grain size data from Watt (2003).

averages 11m. The calcareous species Ammonia tepida, Elphid-iella hannai, and Elphidium excavatum are dominant, whereasthe agglutinated trochamminids (Trochammina inflata, T.kellettae, T. macrescens, and T. pacifica) are common. Onceagain, this association resembles the Post-Invasion IntermediateSubtidal Biofacies, except for the absence of Trochamminahadai.

Wagner’s (1978) three grab samples obtained in the deep waters(mean = 32m) between Alcatraz Island and the Golden GateBridge form the last cluster (text-figs. 10, 11). These samplesare characterized by abundant Elphidiella hannai (9–43%; Ta-ble 6) and common Elphidium. Ammonia tepida occurs in lowabundance (2–14%), whereas Trochammina kellettae accountsfor as much as 26% of the fauna. Marine-indicating species arealso present, including Buccella tenerrima, some species ofTrochammina, and Rosalina globularis (1–49%). With a mix-ture of deep estuarine and marine faunal elements, this Pre-In-vasion Deep Subtidal Biofacies resembles the similarly namedpost-invasion assemblage, but like the Pre-Invasion Intermedi-ate Subtidal Biofacies, it too is devoid of Trochammina hadai.

The dendrogram’s clear separation of samples before and afterthe arrival of Trochammina hadai illustrates the significant im-pact this invasive species has had on the foraminiferal fauna ofSan Francisco Bay’s Central Bay.

CONCLUSIONS

Samples collected in 1998 reveal that four distinct foraminiferalbiofacies occupy the subembayment of San Francisco Bayknown as Central Bay. The agglutinated species Ammobaculitesexiguus, Miliammina fusca, Trochammina inflata and T.macrescens dominate the marshes, while Ammonia tepida ismost abundant in the warmer water at intermediate depths,Elphdium excavatum prefers the cooler water surroundingAlcatraz Island, and Elphidiella hannai associates with the coldmarine water in the western part of Central Bay. Just 15 yearsafter its introduction, the non-native species Trochamminahadai dominates the warmest and shallowest eastern parts of thebay, where it comprises 68-97% of the foraminiferal fauna. Thefour biofacies differentiated by cluster analysis reflect tidal flowintensity, water temperature, degree of marine influence, andthe relative abundance of T. hadai. A comparison of these

538


TABLE 6

Abundances of benthic foraminifera in Central Bay samples collected from 1930 to 1997. Presence/absence data provided for McDonald and Diediker(1930), and percentage of total foraminifera/sample in those collected by Means (1965), Locke (1971), Wagner (1978), Sloan (1980-1981, unpublisheddata), and SFEI (McGann and Sloan 1999). Samples marked with an asterisk are adjusted for removal of planktic specimens. No faunal counts were re-ported by Means for samples M-27 and M-28 or by Wagner for samples W-2675, W-2676, and W-2677. Depth of Means’samples approximated based onbottom topography map (Means 1965) and recent USGS investigations (McGann et al. 2013). FN = Foraminiferal Number (number of foraminiferalspecimens/gram dry sediment).

biofacies before and after the arrival of T. hadai illustrates thatthis invasive species has had a major impact on theforaminiferal fauna of Central Bay.

ACKNOWLEDGMENTS

I would particularly like to thank Doris Sloan (University ofCalifornia, Berkeley) for valuable discussions regarding the en-vironmental factors affecting foraminiferal distributions inCentral Bay. I would also like to thank Steve Watt for the grainsize data, Don Woodrow (USGS) for discussions and the sedi-mentological data, and Brian Reed for technical support. Thismanuscript greatly benefited by reviews kindly provided byKenneth Finger (University of California Museum of Paleon-tology), Amy Lesen (Dillard University), Charles Powell II(USGS), and Doris Sloan.

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Late 20th Century benthic foraminiferal distribution … · Late 20th Century benthic foraminiferal distribution in Central San Francisco Bay, California: Influence of the Trochammina