Sediment organic matter composition and dynamics in...

Estuarine, Coastal and Shelf Science 66 (2006) 501e512www.elsevier.com/locate/ecss

Sediment organic matter composition and dynamicsin San Francisco Bay, California, USA: Seasonal variation

and interactions between water column chlorophyll and the benthos

Amy E. Lesen*

Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, CA 94720, USA

Received 25 August 2003; accepted 4 October 2005

Available online 6 December 2005

Abstract

Sediment and water column data from four sites in North, Central and South San Francisco Bays were collected monthly from November1999 through November 2001 to investigate the seasonal variation of benthic organic matter and chlorophyll in channel sediments, the compo-sition and quality of sediment organic matter (SOM), and the relationship between seasonal patterns in benthic organic matter and patterns inwater column chlorophyll. Water column chlorophyll peaked in the spring of 2000 and 2001, characteristic of other studies of San Francisco Bayphytoplankton dynamics, however an unusual chlorophyll peak occurred in fall 2000. Cross-correlation analysis revealed that water columnchlorophyll at these four channel sites lead sediment parameters by an average of 2 to 3 months. Sediment organic matter levels in the SanFrancisco Bay channel showed seasonal cycles that followed patterns of water column production: peaks in water column chlorophyll were fol-lowed by later peaks in sediment chlorophyll and organic matter. Cyclical, seasonal variations also occurred in sediment organic matter param-eters with sediment total organic carbon (TOC) and total nitrogen (TN) being highest in spring and lowest in winter, and sediment amino acidsbeing highest in spring and summer and lowest in winter. Sediment chlorophyll, total organic carbon, and nitrogen were generally positivelycorrelated with each other. Sediment organic matter levels were lowest in North Bay, intermediate in Central Bay, and highest in South Bay.C:N ratio and the ratio of enzyme hydrolyzable amino acids to TOC (EHAA:TOC) data suggest that SOM quality is more labile in Centraland northern South Bay, and more refractory in North Bay and southern South Bay.� 2005 Elsevier Ltd. All rights reserved.

Keywords: organic matter composition; organic matter dynamics; seasonal variation; chlorophyll; benthos; water column

1. Introduction

The sources and dynamics of organic matter in estuariesand coastal systems are important ecological problems thathave occupied researchers for many years (Tietjen, 1968;Bryan, 1979; Spiker, 1981; Odum, 1984; Smith et al.,1989; Jassby et al., 1993; Deegan and Garritt, 1997; Zimmer-man and Canuel, 2001). Some particular sources of interesthave been the relative contributions of the water column

* Present address: Department of Math and Science, Pratt Institute, 200 Wil-

loughby Avenue, Brooklyn, NY 11205, USA.

E-mail address: [email protected]

0272-7714/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2005.10.003

and benthos, and the interactions between pelagic and benthiccomponents of estuarine systems (‘‘benthic-pelagic cou-pling’’) (Asmus et al., 1992; Noji et al., 1993; Hopkinsonet al., 1998; Vidal and Morgui, 2000). Organic matter andprimary production originating in the water column havebeen documented to have major bearing on many benthiccharacteristics in estuaries including organic matter levelsin sediment, benthic metabolism and flux, and the ecologyand life histories of benthic organisms (Thompson and Nich-ols, 1988; Schlacher and Wooldridge, 1996; Sagan and Thou-zeau, 1998; Zimmerman and Canuel, 2001). Similarly,researchers have shown that physical, chemical, and biologi-cal processes in the benthos can have key impacts on a wealthof pelagic qualities such as nutrient levels, phytoplankton

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502 A.E. Lesen / Estuarine, Coastal and Shelf Science 66 (2006) 501e512

biomass and water column chlorophyll concentration, and mi-crobial loop activity (Cloern, 1982; Middelboe et al., 1998;Hopkinson et al., 1999). Considerable spatial and seasonalvariation in the composition and sources of suspended partic-ulate organic matter (SPM) as well as sediment organic mat-ter (SOM) has been documented in estuaries globally (Canueland Martens, 1993, 1996; Middelburg and Nieuwenhuize,1998; Canuel and Zimmerman, 1999; Hedges and Keil,1999; Zimmerman and Canuel, 2001; Schafer et al., 2002).Canuel and Zimmerman (1999) and Zimmerman and Canuel(2001) related SOM composition to water column parametersand SPM composition in Chesapeake Bay, USA. Canuel andMartens (1993, 1996) examined seasonal changes in SOMcomposition in response to delivery and diagenesis. Harveyand Johnston (1995) compared the lipid biomarker composi-tion of sinking and size-fractionated particulate organic mat-ter (POM). These studies have given us valuable informationabout organic matter cycling in estuaries, however, more re-search into seasonal variations in benthic organic matterand benthic-pelagic relationships are needed to completethe picture.

San Francisco Bay is a large, shallow, temperate estuaryand is one of many such systems worldwide characterizedby light-limitation, high nutrients, and low chlorophyll(Monbet, 1991; Jassby et al., 2002). San Francisco Bay hasa substantial historical oceanographic data set and some welldocumented benthic-pelagic interactions (Cloern, 1996). Thehistory of ecological research and availability of long-termdata in San Francisco Bay thus make it an ideal system inwhich to further explore outstanding questions about sedimentorganic matter cycling in light-limited, low chlorophyllestuaries.

Seasonal cycles in sediment chlorophyll have been docu-mented in the San Francisco Bay system, (Nichols andThompson, 1985; Grenz et al., 2000), as have differencesin microphytobenthos photosynthetic production between dif-ferent regions of the bay (Guarini et al., 2002). Existing dataon seasonal cycles in sediment chlorophyll-a in San Fran-cisco Bay do not differentiate between water column andbenthic sources of primary production, therefore quantitativeknowledge of the relative importance of settling phytoplank-ton and in-situ production in the channel versus the shoals,and at different times of year, is limited (Nichols and Thomp-son, 1985; Grenz et al., 2000). Thus, while many aspects ofprimary production and organic carbon cycling have beenstudied, questions remain concerning the sources of benthicorganic matter, the quantitative nature of benthic primaryproduction, and the dynamics and composition of sedimentorganic matter (Nichols and Thompson, 1985; Guariniet al., 2002).

In this study, 2 years of sediment and water column datafrom four sites in North, Central and South San FranciscoBays are used to investigate the seasonal variation of organicmatter and chlorophyll in channel sediments, between-site dif-ferences in sediment organic matter, and the relationship be-tween seasonal patterns in benthic organic matter andpatterns in water column chlorophyll.

2. Materials and methods

2.1. Environmental setting and study sites

San Francisco Bay is a shallow, turbid embayment with anaverage depth of only 6 m at mean lower low water. The ba-thymetry of the bay is largely characterized by extensive shal-low areas that are cut by deeper channels of 10e20 m(Conomos et al., 1985). San Francisco Bay consists of two hy-drologically distinct (but connected) subsystems (Conomos,1979) (Fig. 1): North San Francisco Bay and South San Fran-cisco Bay. North San Francisco Bay (referred to hereafter as‘‘North Bay’’) is hydrodynamically and biologically character-istic of partially mixed estuaries, and is dominated by the in-fluence of the San Joaquin and Sacramento Rivers. NorthBay consists of two major sub-embayments: Suisun Bay,which is closest to the mouths of the San Joaquin and Sacra-mento Rivers and has the most riverine influence, and San Pa-blo Bay, which is downstream from Suisun Bay andexperiences a combination of riverine and oceanic influence.South San Francisco Bay (hereafter ‘‘South Bay’’) is a tidallyinfluenced, partly enclosed lagoon-type estuary which hasnearly oceanic salinity in the dry summers that decreases dur-ing the high flow winter and spring season. Central San Fran-cisco Bay (hereafter ‘‘Central Bay’’), where North and SouthBay meet, is closest to the site of ocean exchange and experi-ences the most oceanic influence of any part of the bay. SanFrancisco Bay is the largest estuary on the Pacific Coast ofthe Americas, with a surface area of 1240 km2. San FranciscoBay is a highly seasonal system and experiences pronouncedcyclic fluctuations in primary production. South Bay is charac-terized by marked spring phytoplankton blooms (Cloern,1996), and North Bay has historically experienced springand summer blooms (Cloern et al., 1985). These blooms areamongst the most ecologically important characteristics ofseasonal cycles in the bay, and have a major effect on thechemical and biological processes in San Francisco Bay(Cloern et al., 1985).

This study focuses on four sites in San Francisco Bay: onesite in North Bay, (USGS station 12.5); one site in Central Bay(USGS station 17.5); and two stations in South Bay (USGSstations 25 and 28) (Fig. 1). Station 12.5 in the North Bay isthe most influenced by freshwater inflow (Table 1) (USGS,2003). Station 25 is close to the San Bruno Shoal, an importantbathymetric feature of South Bay that affects exchange be-tween Central Bay and the southern part of South Bay.

2.2. Sampling

Sampling was carried out on monthly cruises for a 2-yearperiod from November 1999 through November 2001 in coop-eration with the United States Geological Survey (USGS) onthe R/V Polaris (Table 2).

Water column chlorophyll data were collected on eachcruise by USGS scientists using a CTD with sensors for mea-suring chlorophyll (Sea-Tech in vivo fluorometer) (USGS,2003). CTD chlorophyll data were calibrated on each

503A.E. Lesen / Estuarine, Coastal and Shelf Science 66 (2006) 501e512

Fig. 1. Map of San Francisco Bay showing location of USGS sampling stations used in this study.

sampling date with discrete water measurements sampled bypump or bottles and analyzed in the laboratory for chlorophyllconcentration using chlorophyll extracted in acetone and mea-suring absorption on a Turner Design 10-AU fluorometer(USGS, 2003). Benthic sediment samples were collected usinga 0.10-m2 Van Veen grab.

2.3. Collection and analysis of sediment parameters

Five sediment parameters were measured: sediment chloro-phyll-a, sediment bacterial abundance, sediment amino acids,total organic carbon (TOC) content, and total nitrogen (TN)content of the sediment. The top 1e2 cm of surface sedimentwas collected from the bottom grab at each site. Immediatelyafter collection, aliquots of fresh sediment were homogenizedbriefly, fixed in diluted formalin, and kept at 4 �C for laterbacterial analysis (Turley and Hughes, 1992, 1994). Addition-al aliquots of fresh sediment for chlorophyll analysis were

stored in the dark at 4 �C, and each sample was filtered within24 h. The remainder of the sediment was frozen at �20 �C,freeze dried and stored at room temperature until used in ad-ditional analyses.

Total sediment bacterial abundance was measured using anacridine orange, direct-counting method modified from severalother studies which included sonication of sediment samples(with 10-s pulses and 20-s pauses over a 10-min total period)

Table 1

Sampling stations used in this study. Sampling was carried out on the USGS

R/V Polaris

Station

(USGS #)

12.5 17.5 25 28

Surface salinity

range (PSU)

10e25 20e30 15e32 15e32

Average

depth (m)

6.7 23 8.8 16.2

Location

(coordinates)

38 �2.4# N,

122 �18.9# W

37 �51.755# N,

122 �24.141# W

37 �40.2# N,

122 �19.5# W

37 �#36.1# N,

122 �16.2# W


to dislodge bacteria from the mineral grains (Hobbie et al.,1977; Velji and Albright, 1986; Van Duyl and Kop, 1990; Veljiand Albright, 1993). Sediment chlorophyll was extracted inacetone using the methods of Levinton and McCartney(1991) and read on a Turner Design 10-AU fluorometer.

Freeze-dried sediments were used in analyses of sedimentaryamino acids, total organic carbon, and organic nitrogen. Allfreeze-dried sediment was sieved through a 500-mm sieve be-fore analysis to remove large shell fragments and other debris.Enzyme hydrolyzable amino acid (EHAA) concentrations ofsediments were determined using the methods of Mayeret al. (1995). Additionally, EHAA values were normalized tosediment TOC in order to minimize the influence of be-tween-station differences in sediment grain size, using the fol-lowing calculation: EHAA-C:TOC (Mayer, personalcommunication). Total sediment organic carbon (TOC) and to-tal nitrogen (TN) were determined using a Fisons NS 1500 Se-ries 2 Elemental analyzer using acetanilide and atropine asstandards. For very low peaks of nitrogen, peaks were integratedby hand to get a reliable value. The detection limit for theTOC/TN method was 0.014% for the TOC analysis and0.004% for the TN analysis. Sediment was acidified with 0.3 MHCl to remove carbonates prior to carbon and nitrogen analysis.

3. Results

Water column chlorophyll-a values represent averages forthe entire water column (USGS, 2003). Due to logisticalchanges in water column sampling, there were some monthsduring the study period when water column chlorophyll datawere not available for Station 12.5, 17.5, or 28 (Station 12.5from February 2000 to December 2000; Station 17.5 for sum-mer and fall 2000; Station 28 for spring and summer 2000).For these months, water column data from nearby Stations12, 17 and 29, respectively, were used (Fig. 1) (USGS, 2003).

3.1. North Bay: Station 12.5

Water column chlorophyll-a at Station 12.5 showed seasonaltrends with maxima in the spring of both study years. Mean

Table 2

Sampling dates for this study, USGS R/V Polaris

Sampling date

1999 2000 2001

11e12 January

8e9 February 6e7 February

7e8 March 26e27 February

4e5 April 27e28 March

16e17 May 24e25 April

13e14 June 24e25 May

11e12 July 19e20 June

8e9 August 17e18 July

5e6 September 11e12 September

10e11 October 15e16 October

10e11 November 7e8 November 27e28 November

14e15 December 12e13 December

water column chlorophyll-a at Station 12.5 during the studyperiod was 3.2 mg m�3, with peaks of 15.8 mg m�3 in April2000 and 6.3 mg m�3 in April 2001 (Fig. 2).

Sediment chlorophyll-a, sediment TOC and sediment nitro-gen were all highest during July 2000 and June/July 2001(Fig. 2). Sediment TOC values were highest in July 2001 at1.4 � 0.08% and November 2001 at 1.2 � 0.02%, while TNpeaked in November 2000 at 0.57 � 0.08% and0.13 � 0.01% in November 2001. All sediment variables (ex-cept bacterial abundance) showed an increase at the end of thestudy period in November 2001. Grain size of the sediment atStation 12.5 was course to medium sand, and had the morecourse grain-size of all the stations used in this study. The sed-iment was made up mostly of large grains of quartz-likeminerals.

Peaks in water column chlorophyll-a lead peaks in sedi-ment chlorophyll-a ( p ¼ 0.027) and sediment TOC( p ¼ 0.032) by 2e3 months (cross-correlation analysis, SY-STAT v. 10.2.01, a ¼ 0.05). The sediment time series datawas smoothed using a running median smooth algorithm andthe smoothed data then tested for correlations between param-eters. Sediment chlorophyll-a was positively correlated withTOC ( p ¼ 0.049) and nitrogen ( p ¼ 0.003, Table 3), andEHAA was positively correlated with bacteria ( p < 0.001, Ta-ble 3). C:N ratios of sediment at Station 12.5 ranged from 6.2

Sediment chlorophyll-a

ug g

-1

01234

Sediment bacteria

Nov20001999 2001

Jan Mar May Jul Sep Nov

Month

Jan Mar May Jul Sep Nov

# g-1

08e+62e+72e+73e+7

Sediment total organic carbon

%

0.0

0.6

1.2

1.8

Sediment amino acids

mg

g-1

0.0

0.2

0.4

0.6

mg

m-3

05

101520

%

0.00

0.07

0.14

0.21 Sediment nitrogen

Water column chlorophyll-a

Fig. 2. Water column and sediment values USGS Station 12.5, North San Fran-

cisco Bay, November 1999 though November 2001.


to 27.0 with lowest values in spring and summer 2000, andhighest values in spring 2001 and fall 1999.

3.2. Central Bay: Station 17.5

Mean water column chlorophyll-a at Station 17.5 duringthe study period was 3.18 mg m�3, with peaks in March2000 of 5.72 mg m�3 and in April 2001 of 11.5 mg m�3

(Fig. 3).Sediment chlorophyll-a was lowest in winter 2000e2001

with an average value during December 2000, January 2001and February 2001 of 0.56 mg m�3, while values for the rest

Table 3

Pearson correlations between sediment parameters (median-smoothed data) at

North Bay Station 12.5, with Bonferroni adjusted probabilities. SYSTAT v.

10.2.01. *Correlations that are significant at a ¼ 0.05

Chl-a Bacteria TOC Nitrogen

r p r p r p r p

Bacteria 0.111 1.000 e e e e e eTOC 0.575 0.049* �0.638 0.012* e e e e

Nitrogen 0.685 0.003* 0.167 1.000 0.437 0.489 e e

EHAA 0.427 0.559 0.311 1.000 0.292 1.000 0.285 1.000

0

4

8

12

0.00

0.25

0.50

0.75

%

0.0

0.4

0.8

1.2

0

1e+7

2e+7

3e+7

0

5

10

15

%

0.00

0.04

0.08

0.12

mg

m-3

ug

g-1

#

g-1

mg

g-1




Sediment nitrogen


Sediment bacteria

Nov Jan Mar May Jul Sep Nov Jan Mar May Jul Sep Nov2000

Month1999 2001

Fig. 3. Water column and sediment values USGS Station 17.5, Central San

Francisco Bay, November 1999 though November 2001.

of the year averaged between approximately 2.0 and6.0 mg m�3 (Fig. 3). Sediment amino acids peaked slightlyin spring of both study years, with values of 0.33 and0.39 mg g�1 in April 2000 and May 2001 respectively(Fig. 3). Sediment TOC and nitrogen values were lowest infall 2000, with TOC at 0.07 � 0.03% in October 2000 and ni-trogen at 0.02 � 0.006%, in August 2000 (Fig. 3). Sedimentquality at Station 17.5 was medium to fine sand, slightly finerthan the grain size at Station 12.5.

Analysis of median-smoothed data showed that water col-umn chlorophyll-a at Station 17.5 was strongly and positivelycorrelated with water column chlorophyll-a at North Bay Sta-tion 12.5 (SYSTAT v. 10.2.01, Pearson correlation with Bon-ferroni probabilities, p � 0.001). Cross-correlation analysisdid not reveal any statistically significant correlations betweenwater column chlorophyll-a and sediment parameters at Sta-tion 17.5.

Analysis of median-smoothed data revealed sediment nitro-gen and TOC were positively correlated ( p ¼ 0.001), as wereamino acids and TOC ( p ¼ 0.008, Table 4). C:N ratios of sed-iment at station 17.5 ranged from 4.5 to 13.7 with lowest val-ues in spring 2000 and highest values in winter and summer2000.

3.3. South Bay: Station 25

Mean water column chlorophyll at Station 25 was7.61 mg m�3. There were peaks in chlorophyll-a during thespring bloom period of 15.0 mg m�3 in April 2000 and30.3 mg m�3 and 13.8 mg m�3 in March and April 2001, re-spectively (Fig. 4). There was also a strong phytoplanktonbloom in South Bay in fall 2000: water column chlorophyll-a levels at Station 25 were 26.0 and 33.0 in November and De-cember 2000, respectively. Sediment parameters peaked in thespring/summer, and in some cases, fall (Fig. 4). Sedimentchlorophyll-a peaked slightly in January 2000 (7.02 mg m�3)and spring 2001 (4.76 mg m�3 in May 2001) (Fig. 4). Therewas a more pronounced peak of sediment chlorophyll-a,12.1 mg m�3, in September 2001 (Fig. 4). Sediment TOCand nitrogen peaked in spring 2000 and 2001, with TOC val-ues at 1.2 � 0.02%, in April 2000 and 1.6 � 0.72%, in April2001, and nitrogen values at 0.13 � 0.001%, in April 2000and 0.11 � 0.006%, in April 2001 (Fig. 4). The sediment grainsize at Station 25 was silty in quality, with much finer grainsize than Stations 12.5 or 17.5. There were no significant

Table 4


Central Bay Station 17.5, with Bonferroni adjusted probabilities. SYSTAT v.



r p r p r p r p

Bacteria 0.397 0.823 e e e e e e

TOC 0.371 1.000 �0.396 0.829 e e e eNitrogen 0.395 0.841 �0.186 1.000 0.735 0.001* e e

EHAA 0.496 0.206 0.079 1.000 0.652 0.008* 0.453 0.394


correlations between water column chlorophyll-a and sedi-ment parameters at Station 25.

Visual examination of the data suggests that peaks in sedi-ment parameters lag peaks in water column chlorophyll-a byone to four months, and cross-correlation analysis shows a pos-itive correlation between water column chlorophyll-a and sed-iment amino acids with peaks in sediment amino acids laggingwater column chlorophyll-s by four months (cross-correlationanalysis, SYSTAT v. 10.2.01, a ¼ 0.05, p ¼ 0.028).

Analysis of median smoothed data reveals that sedimentTOC shows a strong correlation with nitrogen ( p � 0.001)and amino acids ( p � 0.001), and nitrogen is strongly correlatedwith amino acids ( p � 0.001, Table 5). C:N ratios of sedimentat Station 25 ranged from 4.6 to 13.5, with lowest values inlate summer and fall 2000 and highest values in spring 2001.

3.4. South Bay: Station 28

South Bay Station 28 showed similar trends to Station 25.Mean water column chlorophyll was 10.09 mg m�3. Strongspring water column chlorophyll-a peaks occurred:14.3 mg m�3 and 25.5 mg m�3 in March and April 2000, re-spectively, and 35.0 mg m�3 and 40.9 mg m�3 in March andApril 2001 (Fig. 5). Station 28 also showed a fall 2000 bloom

0

5

10

15

-1

0

1

2

3

0.0

0.5

1.0

1.5

0

1e+7

2e+7

3e+7

010203040

0.00

0.07

0.14

0.21




Sediment bacteria


Sediment nitrogen

%%

mg

m-3

ug

g-1

m

g g-1

#

g-1

Nov Jan Mar May Jul Sep Nov

Month

Jan Mar May Jul Sep Nov20001999 2001

Fig. 4. Water column and sediment values USGS Station 25, South San Fran-


with water column chlorophyll-a peaks of 41.5 mg m�3 and20.4 mg m�3 in November and December 2001, respectively.

All sediment parameters (except bacterial abundance)peaked in the spring. Sediment chlorophyll-a was10.4 mg m�3 in April 2000 and 23.9 mg m�3 in March 2001(Fig. 5). Sediment TOC peaked at 2.6 � 0.04%, in April2000 and 1.6 � 0.03%, in May 2001, while sediment nitrogenpeaked at 0.18 � 0.009%, in May 2000 and 0.18 � 0.002%, inJune 2001 (Fig. 5). Sediment amino acids peaked at 0.52 inMay 2000 and 0.55 in May 2001. The sediment grain sizewas fine silt at Station 28, and the grain size at this stationwas the finest of all the stations used in this study.

Cross-correlation analysis revealed positive correlations be-tween water column chlorophyll and sediment chlorophyll

Table 5


South Bay Station 25, with Bonferroni adjusted probabilities. SYSTAT v.



r p r p r p r p

Bacteria �0.310 1.000 e e e e e eTOC 0.383 0.966 �0.180 1.000 e e e e

Nitrogen 0.512 0.159 �0.184 1.000 0.906 <0.001* e e

EHAA 0.266 1.000 �0.032 1.000 0.764 <0.001* 0.787 <0.001*

0

10

20

30

0

1

2

3

0.0

0.4

0.8

1.2

0

2e+7

4e+7

6e+7

0204060

0.0

0.1

0.2

0.3




Sediment bacteria


Sediment nitrogen

mg

m-3

ug

g-1

m

g g-1

#

g-1

%%

Nov Jan Mar May Jul Sep Nov Jan Mar May Jul Sep Nov20001999 2001

Month

Fig. 5. Water column and sediment values USGS Station 28, South San Fran-



( p ¼ 0.044), sediment nitrogen ( p ¼ 0.015) and sedimentamino acids ( p ¼ 0.039) (cross-correlation analysis, SYSTATv. 10.2.01, a ¼ 0.05). Peaks in water column chlorophyll-a ledpeaks in sediment chlorophyll-a, sediment nitrogen, and sedi-ment amino acids by 3 months.

Analysis of the smoothed data shows a significant positivecorrelation between sediment carbon and nitrogen ( p � 0.001,Table 6). C:N ratios of sediment at Station 28 ranged from 5.9to 17.9 with lowest values in summer 2000 and highest valuesin spring 2000.

4. Discussion

4.1. Water column patterns

The spring patterns observed follow those seen in manypublished studies of phytoplankton bloom dynamics in Northand South Bays (e.g. Cloern et al., 1985; Powell et al., 1989;Cloern, 1996; Lucas et al., 1999). In San Pablo Bay chloro-phyll increased eightfold in April 2000, and threefold in spring2001. In the South Bay, at Station 25 water column chloro-phyll increased sevenfold in April 2000 and tenfold in March2001 (Fig. 4). Station 28 showed an eightfold increase in watercolumn chlorophyll-a in April 2000 and a tenfold increase inApril 2001 (Fig. 5). Station 28 generally showed the highestwater column chlorophyll-a levels of all sites, which is alsoconsistent with published observations that mean phytoplank-ton annual growth rate and primary production are highest inSouth Bay, with chlorophyll-a levels being highest of all inthe southern part of South Bay (Cloern et al., 1985; Powellet al., 1989).

The fall data for South Bay do not show patterns that havebeen typically observed in South San Francisco Bay in the fallin over 20 years of data collection by the United States Geo-logical Survey (Cloern, 1996). At Station 25 in Novemberand December 2000, water column chlorophyll-a levels werean order of magnitude higher than chlorophyll-a values atthe same station in November and December 1999(2.40 mg m�3 and 2.25 mg m�3, respectively) and in Novem-ber and December 2001 (2.60 mg m�3 and 3.30 mg m�3, re-spectively) (USGS, 2003). A similar pattern was observed atStation 28 in November and December 2000 as well. Watercolumn chlorophyll-a levels at Station 28 in November andDecember 2000 were 41.5 mg m�3 and 20.4 mg m�3 respec-tively, while in November and December 1999 values were

Table 6


South Bay Station 28, with Bonferroni adjusted probabilities. SYSTAT v.



r p r p r p r p

Bacteria �0.289 1.000 e e e e e eTOC 0.237 1.000 0.230 1.000 e e e e

Nitrogen 0.042 1.000 0.281 1.000 0.811 <0.001* e e

EHAA 0.088 1.000 0.422 0.598 0.227 1.000 0.398 0.814

2.3 mg m�3 and 2.1 mg m�3 respectively, and in Novemberand December 2001, 3.6 mg m�3 and 3.5 mg m�3 respectively(USGS, 2003). A similar fall bloom pattern in the South Bayhas been seen in subsequent years since 2000, so this phenom-enon was not an anomalous occurrence in fall 2000 (USGS,2003; J.E. Cloern, personal communication).

The causes of these chlorophyll peaks in the fall in SouthBay are not immediately apparent. Amongst the most impor-tant mechanisms known to contribute to creation of the SouthBay spring bloom are: (1) increase in freshwater inflow fol-lowing winter rains, which results in density stratification ofthe water column; (2) interactions between wind, semidiurnaltides, and the spring-neap tidal cycle, which effect spatial andtemporal variations in turbidity and turbulent mixing (for in-stance, the low tidal energy period of the fall equinox in SanFrancisco Bay could result in blooms through these mecha-nisms); (3) lack of benthic grazing (Cloern, 1984, 1991; Ko-seff et al., 1993; Lucas et al., 1998; May et al., 2003). Withthe currently available information, only reason (1) can beeliminated. However, preliminary research suggests that thisfall South Bay bloom is caused by different species of phyto-plankton than those dominating the spring bloom in SouthBay: the 2004 fall bloom was a dinoflagellate bloom thatwas likely to be seeded from offshore. (J.E. Cloern, personalcommunication; J. Thompson, personal communication). Itis possible that the fall bloom in South Bay reflects cyclicityin this system operating at timescales longer than the 20 yearsduring which workers have been studying phytoplanktonbloom dynamics in San Francisco Bay (J.E. Cloern, personalcommunication).

4.2. Water columnesediment relationships

The cross-correlation analyses show significant correlationsbetween water column chlorophyll-a and sediment chloro-phyll-a at Stations 12.5 and 28, with sediment amino acidsat Station 25, and with sediment nitrogen at Station 28. Thesedata indicate that water column chlorophyll at these four chan-nel sites lead sediment parameters by an average of 2e3 months. Some of the organic matter produced in the shoalsduring blooms is transported to the channel where it is con-sumed or deposited into the deep sediments and metabolizedby the benthos (Caffrey et al., 1998).

The bloom periods of 1999 through 2001 show increases insediment parameters that remain high for one to three months(Figs. 2e5). Therefore, depending on sedimentation rates andturnover of organic matter in the benthos, my data suggest thatdeposition of organic material from the water column maycause increases in benthic organic matter that are rapid (attimescales of weeks as found by other workers) but may per-sist for several months (as indicated by the data presentedhere). The timescale, scope, and geographic context of thisstudy is important to note when comparing these data with re-sults from other studies. Grenz et al. (2000) found that in thepost-bloom South Bay, the sediment chlorophyll-a concentra-tion in the shoals was much higher than the water columnchlorophyll-a concentration, suggesting rapid sedimentation


and incorporation of phytoplankton into surface sediments,and that peaks in benthic chlorophyll followed peaks in watercolumn chlorophyll by only 2 weeks. The data presented inthis study, which represent a whole bay gradient rather thanone location, were taken at monthly intervals, therefore thepatterns described here are at longer timescales than the 2e4 weeks found to be important in water columnesediment re-lationships in other studies of San Francisco Bay (Caffreyet al., 1998; Grenz et al., 2000). Studies in other estuariesalso found peaks in sediment chlorophyll three to four weeksafter phytoplankton blooms (Sagan and Thouzeau, 1998). Oneexplanation is that increases in chlorophyll-a begin in the shal-lows (Cloern et al., 1985) and are longer in duration than in-creases in deep water chlorophyll-a. The data presented hereare from the deep channel, therefore transported materialmay reflect pelagic production in the shallows as opposed tothe channel.

Tidal activity has been shown to be important in chloro-phyll dynamics in low chlorophyll, light-limited systems sim-ilar to San Francisco Bay (Monbet, 1991). Anotherexplanation for the sediment-water column relationship re-ported here is that transport from the shallows to the channeloccurs during spring tides (Schoellhamer, 1996; Lacy et al.,2003). If sampling for this study was done on or during an earlyspring tide, the sampling may not have picked up the signalfrom this resuspended material until the following sampledate.

4.3. Sediment patterns

San Francisco Bay in is known to belong to a class of light-limited, low-chlorophyll, high-nutrient systems worldwide(Monbet, 1991; Cloern, 1996). The samples for this studywere all collected in the channel, 6.7e23 m deep, so it is likelythat all the chlorophyll-a in channel sediments is the result ofsedimentation from the water column, rather than in situ ben-thic production. However, in shallow systems such as SanFrancisco Bay, the distinction between phytoplankton and mi-crophytobenthos is often blurred, as phytoplankton can sinkand still photosynthesize, and microphytobenthos can be re-suspended and become part of the phytoplankton (Cahoonet al., 1993; Macintyre et al., 1996). Nichols and Thompson’s(1985) study of benthic microalgae found that the benthic mi-croalgal assemblage was comprised largely of phytoplanktoncells that settled to the bottom following the South Bay bloom,supporting the idea that water column is the source of benthicchlorophyll to channel sediments.

Due to the high turbidity in San Francisco Bay shallows,microphytobenthic primary production is probably largely re-stricted to intertidal areas (Alpine and Cloern, 1988; Guariniet al., 2002). Benthic microalgae is abundant in mats on inter-tidal mudflats in San Francisco Bay (Thompson et al., 1981;Nichols and Thompson, 1985). Jassby et al. (1993) suggestedthat benthic microalgae may be significant contributors to or-ganic carbon in South San Francisco Bay; however, no directmeasurements of photosynthesis by benthic microalgae are re-ported. Guarini et al. (2002) measured microphytobenthic

primary production for intertidal sites in three areas of SanFrancisco Bay at a single point in time, finding significant dif-ferences between the tidal freshwater Delta, North Bay, andSouth Bay with South Bay having the highest carbon assimi-lation rate. This suggests that microphytobenthic productionis more important in certain areas of San Francisco Bay thanin others, and that the relative contribution of microphytoben-thos versus phytoplankton to benthic chlorophyll may changethroughout the year.

In this study, sediment chlorophyll at all stations exhibitedseasonality, generally showing peaks at all stations in the latespring and early summer, with lowest values in the winter(Figs. 2e5). North Bay Station 12.5 showed marked peaksin sediment chlorophyll in late spring and early summer(Fig. 2). Central Bay Station 17.5 was more variable, butalso showed sediment chlorophyll peaks in the late spring orsummer of both years (Fig. 3). At both South Bay Stations25 and 28, almost all sediment parameters exhibited a peak be-tween the fall and spring 2000e2001 blooms, and Station 25experienced a peak in sediment chlorophyll-a after the spring2001 bloom (Figs. 4 and 5). Station 28 sediment parametersgradually increased from June or July 2001 to September2001 (Fig. 5).

There were also between-site differences in sediment chlo-rophyll levels (Table 7). Maximum sediment chlorophyll lev-els increased from north to south, with the highest maximumchlorophyll concentrations found at Station 28 and the lowestfound at Station 12.5 (Table 7). Mean sediment chlorophyll-alevels in Central Bay at Station 17.5 were comparable to thosein northern South Bay at Station 25 (Table 7). Lower chloro-phyll waters from the coastal ocean and Delta dominate atthe northern part of South Bay (Powell et al., 1989). Station25 is just north of San Bruno Shoal, which is a significant bar-rier to exchange between the northern and southern reaches ofSouth Bay, and therefore it receives more influence from Cen-tral Bay than does Station 28 (Cloern, 1996). Differences insediment chlorophyll levels may also be influenced by grainsize. Grain size patterns (which reflect vertical transportrate) exhibited a continuum from largest at Station 12.5 tosmallest at Station 28. Finer grain size is often associatedwith higher organic matter content, so the between-site varia-tions in sediment chlorophyll reported here might also be in-dicative of grain size differences (Canuel and Martens,1996). However, since the north-south gradient in chloro-phyll-a concentration in the water column is identical to thegradient reported here in the sediment, water column chloro-phyll concentration is likely the most significant contributor

Table 7

Sediment chlorophyll-a mean, minimum and maximum measured values dur-

ing the study period of November 1999 through November 2001

USGS Station # Mean chl-a Min chl-a Max chl-a

12.5 1.089 0.042 3.657

17.5 3.500 0.360 8.417

25 2.925 0.197 12.016

28 4.348 0.457 23.932


to this pattern, as opposed to in-situ production or transportrate (Cloern et al., 1985; Powell et al., 1989).

Data presented here demonstrate seasonal variations andbetween-site differences in other types of sediment organicmatter as well (e.g. total organic carbon, nitrogen, and aminoacids) and significant relationships between some of these pa-rameters within the benthos. There were seasonal variations insediment TOC and sediment TN, and between-site differencesin these variables. Sediment TOC was highest at Stations 25and 28 (Figs. 2e5), and generally highest in spring and lowestin winter at all stations. Sediment nitrogen was lowest at Sta-tion 17.5 and highest at Station 28; sediment TN seasonal pat-terns were similar to that of TOC, with peaks in spring andlowest values in the winter (Figs. 2e5). Sediment amino acidsalso showed the between-site patterns: highest EHAA valueswere at Stations 25 and 28, followed by Station 17.5 withthe mid-range values, and 12.5 with the lowest EHAA values(Figs. 2e5). Sediment amino acids generally peaked in springand summer and were lowest in winter, although EHAA valueswere very variable and did not show as marked a seasonal sig-nal as other sediment values such as TOC, TN, and sedimentchlorophyll-a. The peaks of these parameters in the springcould reflect either inputs from the spring phytoplanktonbloom or the accumulation of allochthonous material deposit-ed after the San Francisco Bay Area’s winter rainy season. Theimportance of different inputs to SOM at different times ofyear has been documented in other large estuaries (Sharpet al., 1986; Canuel and Martens, 1993; Zimmerman and Can-uel, 2001). In-situ processes are also important: studies of lipidbiomarkers in Chesapeake Bay sediments suggest that season-al trends in sediment OM quality and composition reflect bothin-situ phenomena such as bacterial-mediated processes, aswell as temporal changes in environmental parameters and riv-erine inputs (Canuel and Martens, 1993).

C:N ratios were generally highest at Station 12.5 (maxi-mum C:N ratio 27), mid-range vat Station 28 (maximum17.9) and lowest at Stations 17.5 and 25 (maximum 13.7and 13.5, respectively). The between-site differences in C:Nratio imply that organic matter sedimented to the benthos atCentral and South Bay Stations 17.5 and 25 may be fresherthan that at North Bay Station 12.5 or South Bay Station 28,which may be reworked in the water column before reachingthe sediment. The largest source of freshwater to the SouthBay in summer is sewage treatment plants. Station 28 is closeto the largest sewage outfall in the bay at San Jose, therefore itis possible that the C:N ratio at Station 28 is being affected bythis source. Fresh material has a lower C:N ratio than detritalmaterial (fresh phytoplankton usually has a ratio of approxi-mately 7.0e7.5, while detritus usually has a C:N of 20e30)(Hedges et al., 1988). Additionally, macrophytes and pelagicdiatoms may have higher C:N ratios under some conditions,whereas OM derived from benthic diatoms may have lowerC:N signatures (Fry and Wainwright, 1991; Stribling andCornwell, 1997). Combinations of macrophyte and benthic al-gae sources may balance each other and make sources of SOMdifficult to resolve (Zimmerman and Canuel, 2001). However,the mean station C:N ratios were not statistically significantly

different from each other (ANOVA, SYSTAT v. 10.2.01,a ¼ 0.05). Without stable isotope or lipid biomarker data,the sources of the SOM cannot be determined in this case.

The differentials in C:N ratios could be explained by grainsize differences; the sandy sediment quality in North Bay alsolikely contributes to low sediment nitrogen levels, whichwould result in high C:N ratios. The between-site patternsshown in the data (highest SOM levels in the South Bay, inter-mediate values in the Central Bay, and lowest values in theNorth Bay) may reflect grain size differences to a greater ex-tent than they reflect regional differences in organic matter in-puts and water column phytoplankton production. EHAA isa measure of the protein in sediment that is available for diges-tion by benthic organisms (Mayer et al., 1995). However,EHAA includes a labile and refractory component, and the re-fractory component is sensitive to grain size (L. Mayer, per-sonal communication). To test the hypothesis that grain sizewas having a large influence on TOC, TN, and C:N values,EHAA values were normalized to TOC in order to reducethe influence of between site grain size TOC differences onEHAA (Table 8). The resulting data show the same patternsat the C:N ratio data. The highest mean EHAA:TOC ratio(0.69 � 1.6) is at Station 25, the next highest is at Station17.5 (0.29 � 0.21), followed by Station 28 (0.17 � 0.12) andStation 12.5 (0.13 � 0.12) (Table 8). These patterns implythat the trends seen in the C:N data are real, and that sedimentorganic matter at Stations 25 and 17.5 is more labile, and thatsediment organic matter at Stations 12.5 and 28 is more

Table 8

Monthly and mean TOC-normalized enzyme hydrolyzable amino acids

(EHAA) for each Station for the study period of November 1999 through

November 2001

EHAA-C:TOC

Station 12.5 Station 17.5 Station 25 Station 28

Nov-99 0.13 0.34 0.41 0.24

Dec-99 0.14 0.23 0.34 0.14

Jan-00 0.02 0.06 0.25 0.05

Feb-00 0.02 0.05 0.05 0.05

Mar-00 0.02 0.09 0.05 0.05

Apr-00 0.10 0.30 0.19 0.07

May-00 0.22 0.55 0.20 0.23

Jun-00 0.17 0.36 0.35 0.17

Jul-00 0.10 0.32 0.13 0.12

Aug-00 0.21 0.34 3.27 0.22

Sep-00 0.22 0.79 7.87 0.31

Oct-00 0.24 1.09 0.38 0.19

Nov-00 0.19 0.13 0.25 0.21

Dec-00 0.11 0.20 0.23 0.27

Jan-01 0.11 0.30 0.56 0.25

Feb-01 0.16 0.22 0.20 0.19

Mar-01 0.12 0.14 0.22 0.14

Apr-01 0.14 0.19 0.18 0.14

May-01 0.12 0.25 0.27 0.17

Jun-01 0.07 0.16 0.18 0.15

Jul-01 0.11 0.15 0.39 0.13

Sep-01 0.09 0.29 0.33 0.17

Oct-01 0.10 0.26 0.26 0.15

Nov-01 0.11 0.15 0.20 0.14

Mean 0.13 0.29 0.69 0.17


refractory. However, it should be noted that the variance isvery high and the mean station EHAA:TOC ratios were notstatistically significantly different from each other (ANOVA,SYSTAT v. 10.2.01, a ¼ 0.05).

As mentioned earlier, sediment chlorophyll-a values werealso similar at Stations 17.5 and 25. Therefore, the EHAA:-TOC and C:N data again point to that fact that Central Bayand northern South Bay, represented here by Stations 17.5and 25, are more hydrodynamically similar to each otherthan are northern South Bay and southern South Bay, Stations25 and 28 (Cloern, 1996).

Marked, cyclical, seasonal variations in chlorophyll in SanFrancisco Bay sediments, such as the ones reported here, havebeen demonstrated in other studies as well (Nichols andThompson, 1985; Grenz et al., 2000; Guarini et al., 2002).The present study is also consistent with other studies thathave shown South Bay to have higher levels of sediment chlo-rophyll than North Bay (Guarini et al., 2002). Guarini et al.(2002) measured microphytobenthic primary production forintertidal sites in three areas of San Francisco Bay at a singlepoint in time, finding significant differences between the Del-ta, North Bay, and South Bay with South Bay having the high-est carbon assimilation rate. Unlike other studies of sedimentdynamics in San Francisco Bay, the data presented here arefor a suite of sediment organic matter parameters, includingthe first sediment amino acid and sediment bacteria data forSan Francisco Bay.

All sediment parameters at all stations were generally pos-itively correlated with each other (Tables 3e6). Increased sed-imentation of labile organic matter to the benthos after SouthBay blooms can result in rapid benthic mineralization of phy-toplankton biomass, and high rates of release of inorganic N,P, and Si from the benthos (Grenz et al., 2000). The positivecorrelations between sediment parameters suggest that theprocesses resulting in increases in sediment chlorophyll im-pact other aspects of the benthos as well, and that these pro-cesses are linked mechanistically.

Bacteria were an exception to this pattern and were oftennegatively correlated with sediment chlorophyll and other sed-iment parameters. Many different factors affect bacterial abun-dance (Austin and Findlay, 1989), and bacterial abundance isa function of organic matter availability, growth rates, and pre-dation. Murrell (1999) found seasonal variability in microbialactivity in North Bay and suggested that water column bacte-ria there are dependent on riverine inputs of organic material.Murray et al. (1996), working in North Bay and Central Bay,suggest that differences in the quality of organic matter alongthe salinity gradient in San Francisco Bay may affect bacterio-plankton community composition.

The dynamics in sediment quality reported here have impli-cations for the ecology and community structure of benthicmacroinvertebrates and meiofauna (Thompson and Nichols,1988). In terms of the cyclicity in sediment chlorophyll, sea-sonal fluctuations in food supply to the benthos have beenfound to be correlated with seasonal changes in growth ratesof several species of benthic macroinvertebrates such as the bi-valve Macoma balthica (Nichols and Thompson, 1985;

Thompson and Nichols, 1988). Sobczak et al. (2002) showedthat the mass of labile riverine organic matter is much smallerthan that supplied by the phytoplankton in this system and theseasonality is thus likely to be a function of local or advectedphytoplankton production. However, the relative importanceof phytoplankton versus microphytobenthos as a food sourcehas been investigated only for one benthic species, Potamo-corbula amurensis, the introduced suspension feeding Asianclam that has become extremely abundant in San FranciscoBay (Canuel et al., 1995). Canuel at al. found that phytoplank-ton was the primary food source for P. amurensis, and thatclams may store compounds during the spring phytoplanktonbloom for use in growth and metabolism at other times ofyear. This indicates that the seasonality in sediment chloro-phyll reported in this study, and the timing of depositionfrom the water column to the benthos, directly affects thelife history, growth and metabolism of major benthic faunain this system. The between-site trends in sediment variablesreported here are also relevant for benthic macroinvertebratecommunity structure. In the sediment, the highest EHAAand TOC values were found in South Bay stations 25 and28, and the highest bacterial abundances at station 28 (Figs.4 and 5). These sites correspond with areas of the SouthBay that were found by Lee et al. (2003) to have macroinver-tebrate assemblages characterized by high abundances of de-posit feeders. This suggests that sediment organic matterquality may be as useful as other parameters traditionallyused to define benthic community structure such as sedimentgrain size (Rhoads, 1974).

More research is needed to answer some of the questionsposed here. Future research using stable isotope and biomarkertechniques would help clarify the processes causing the pat-terns reported here. Further work sampling sediment at weeklyor even daily intervals is necessary to thoroughly investigatethe timescales of the relationship between water column andsediment organic matter. If evidence of the fall South Baybloom reported here persists, more research is needed to un-cover the dynamics of this pattern. Information about sourcesand seasonality of benthic organic matter influences our under-standing of the population dynamics and life histories of thebenthic macro- and meiofauna, and more research into theseinteractions is needed in the San Francisco Bay system.More data should be collected in order to confirm theEHAA and TOC trends reported here, and to investigate themechanisms resulting in these between-site differences inSOM quality.

5. Conclusion

The goals of this study were to investigate the seasonal re-lationship between benthic and pelagic organic matter, and thequality, composition, and dynamics of sediment organic matterin a shallow, light-limited temperate estuary. The data pre-sented here reveal that sediment organic matter levels in theSan Francisco Bay channel show seasonal cycles that followpatterns of water column production. Peaks in water columnchlorophyll are generally followed by later peaks in sediment


chlorophyll and organic matter. The role of the shallows insedimenting material to the channel in San Francisco Bay isnot known and needs to be studied further. Cyclical, seasonalvariations also occurred in sediment organic matter parameterswith sediment total organic carbon (TOC) and total nitrogen(TN) being highest in spring and lowest in winter, and sedi-ment amino acids being highest in spring and summer andlowest in winter. Further research is needed to quantify stableisotope and biomarker signatures in San Francisco Bay sedi-ments in order to investigate seasonal and spatial variationsin OM sources, and to clarify the relative importance of in-situ process versus allochthonous inputs. Sediment chloro-phyll, total organic carbon, and nitrogen were generallypositively correlated with each other. Sediment organic matterlevels are generally lowest in North Bay, intermediate in Cen-tral Bay, and highest in South Bay. C:N ratio and EHAA:TOCratio, suggest that SOM quality is more labile in Central andnorthern South Bay, and more refractory in North Bay andsouthern South Bay. The reason for these SOM quality differ-ences is not apparent; more data need to be collected in orderto investigate possible mechanisms and to confirm the trendsreported in this study.

Acknowledgments

Thanks for funding from: the Department of Integrative Bi-ology and the Museum of Paleontology at the University ofCalifornia (UCMP), Berkeley; The Geological Society ofAmerica, The Paleontological Society, and the CushmanFoundation for Foraminiferal Research. Thanks to Jere Lippsand Deborah Penry for advice in designing the study and forreviewing the manuscript. Thanks to many undergraduate labassistants for help with the sediment analyses. Special thanksto the crew and scientific staff of the USGS R/V Polaris forcollaboration in sample collection, and to the Water QualityResearch Group at USGS Menlo Park for generously provid-ing water column data. The manuscript benefited from reviewsby Jan Thompson and two anonymous reviewers. This isUCMP submission #1859.

References

Alpine, A.E., Cloern, J.E., 1988. Phytoplankton growth rates in a light-limited

environment, San Francisco Bay. Marine Ecology Progress Series 44,

167e173.

Asmus, H., Asmus, R.M., Prins, T.C., Dankers, N., Frances, G., Maass, B.,

Reise, K., 1992. Benthic-pelagic flux rates on mussel beds: tunnel and tidal

flume methodology compared. Helgolaender Meeresuntersuchungen 46

(3), 341e361.

Austin, H.K., Findlay, S.E., 1989. Benthic bacterial biomass and production in

the Hudson River Estuary, New York, USA. Microbial Ecology 18 (2),

105e116.

Bryan, J.R., 1979. The Production and Decomposition of Organic Material in

an EstuarydSouthampton Water. Department of Oceanography, South-

ampton University, UK, p. 197.

Caffrey, J.M., Cloern, J.E., Grenz, C., 1998. Changes in production and respi-

ration during a spring phytoplankton bloom in San Francisco Bay, Califor-

nia, USA: implications for net ecosystem metabolism. Marine Ecology

Progress Series 172, 1e12.

Cahoon, L.B., Beretich, G.R., Thomas, C.J., McDonald, A.M., 1993. Benthic

microalgal production at Stellwagen Bank, Massachusetts Bay USA. Ma-

rine Ecology-Progress Series 102 (1e2), 179e185.

Canuel, E.A., Martens, C.S., 1993. Seasonal variations in the sources and al-

teration of organic matter associated with recently-deposited sediments.

Organic Geochemistry 20 (5), 563e577.

Canuel, E.A., Martens, C.S., 1996. Reactivity of recently deposited organic

matter: Degradation of lipid compounds near the sediment-water interface.

Geochimica et Cosmochimica Acta 60 (10), 1793e1806.

Canuel, E.A., Zimmerman, A.R., 1999. Composition of particulate organic

matter in the southern Chesapeake Bay: sources and reactivity. Estuaries

22 (4), 980e994.

Canuel, E.A., Cloern, J.E., Ringelberg, D.B., Guckert, J.B., Rau, G.H., 1995.

Molecular and isotopic tracers used to examine sources of organic matter

and its incorporation into the food webs of San Francisco Bay. Limnology

and Oceanography 40 (1), 67e81.

Cloern, J.E., 1982. Does the benthos control phytoplankton biomass in South

San Francisco Bay? Marine Ecology Progress Series 9, 191e202.

Cloern, J.E., 1984. Temporal dynamics and ecological significance of salinity

stratification in an estuary, South San-Francisco Bay USA. Oceanologica

Acta 7 (1), 137e140.

Cloern, J.E., 1991. Tidal stirring and phytoplankton bloom dynamics in an es-

tuary. Journal of Marine Research 49 (1), 203e221.

Cloern, J.E., 1996. Phytoplankton bloom dynamics in coastal ecosystems:

A review with some general lessons from sustained investigation

of San Francisco Bay, California. Reviews of Geophysics 34 (2),

127e168.

Cloern, J.E., Cole, B.E., Wong, R.L.J., Alpine, A.E., 1985. Temporal dynamics

of estuarine phytoplankton: a case study of San Francisco Bay. Hydrobio-

logia 129, 153e176.

Conomos, T.J. (Ed.), 1979. San Francisco Bay: The Urbanized Estuary. Inves-

tigations into the Natural History of San Francisco Bay and Delta With

Reference to the Influence of Man. Pacific Division of the American As-

sociation for the Advancement of Science, San Francisco.

Conomos, T.J., Smith, R.E., Gartner, J.W., 1985. Environmental setting of San

Francisco Bay, California, USA. Hydrobiologia 129 (1), 1e12.

Deegan, L.A., Garritt, R.H., 1997. Evidence for spatial variability in estuarine

food webs. Marine Ecology Progress Series 147 (1e3), 31e47.

Fry, B., Wainwright, S.C., 1991. Diatom sources of 13C-rich carbon in marine

food webs. Marine Ecology Progress Series 76, 149e157.

Grenz, C., Cloern James, E., Hager Stephen, W., Cole Brian, E., 2000. Dynam-

ics of nutrient cycling and related benthic nutrient and oxygen fluxes dur-

ing a spring phytoplankton bloom in South San Francisco Bay (USA).

Marine Ecology-Progress Series 197, 67e80.

Guarini, J.-M., Cloern James, E., Edmunda, J., Gros, P., 2002. Microphyto-

benthic potential productivity estimated in three tidal embayments of the

San Francisco Bay: a comparative study. Estuaries 25 (3), 409e417.

Harvey, H.R., Johnston, J.R., 1995. Lipid composition and flux of sinking and

size-fractionated particles in Chesapeake Bay. Organic Geochemistry 23

(8), 751e764.

Hedges, J.I., Keil, R.G., 1999. Organic geochemical perspectives on estuarine

processes: sorption reactions and consequences. Marine Chemistry 65,

55e65.

Hedges, J.I., Clark, W.A., Cowie, G.L., 1988. Organic matter sources to the

water column and surficial sediments of a marine bay. Limnology and

Oceanography 33 (5), 1116e1136.

Hobbie, J.E., Daley, R.J., Jasper, S., 1977. Use of nuclepore filters for counting

bacteria by fluorescence microscopy. Applied and Environmental Microbi-

ology 33 (5), 1225e1228.

Hopkinson Jr., C.S., Giblin, A.E., Garritt, R.H., Tucker, J., Hullar, M.A.J.,

1998. Influence of the benthos on growth of planktonic estuarine bacteria.

Aquatic Microbial Ecology 16 (2), 109e118.

Hopkinson Jr., C.S., Giblin, A.E., Tucker, J., Garritt, R.H., 1999. Benthic me-

tabolism and nutrient cycling along an estuarine salinity gradient. Estuaries

22 (4), 863e881.

Jassby, A.D., Cloern James, E., Powell Thomas, M., 1993. Organic carbon

sources and sinks in San Francisco Bay: variability induced by river

flow. Marine Ecology-Progress Series 95 (1e2), 39e54.


Jassby, A.D., Cloern, J.E., Cole, B.E., 2002. Annual primary production: Pat-

terns and mechanisms of change in a nutrient-rich tidal ecosystem. Lim-

nology and Oceanography 47 (3), 698e712.

Koseff, J.R., Holen, J.K., Monismith, S.G., Cloern, J.E., 1993. Coupled effects

of vertical mixing and benthic grazing on phytoplankton populations in

shallow, turbid estuaries. Journal of Marine Research 51 (4), 843e868.

Lacy, J.R., Stacey, M.T., Burau, J.R., Monismith, S.G., 2003. Interaction of lat-

eral baroclinic forcing and turbulence in an estuary. Journal of Geophysical

Research. C. Oceans 108 (C3).

Lee II, H., Thompson, B., Lowe, S., 2003. Estuarine and scalar patterns of in-

vasion in the soft-bottom benthic communities of the San Francisco Estu-

ary. Biological Invasions 5 (1e2), 85e102.

Levinton, J.S., McCartney, M., 1991. Use of photosynthetic pigments in sedi-

ments as a tracer for sources and fates of macrophyte organic matter. Ma-

rine Ecology-Progress Series 78 (1), 87e96.

Lucas, L.V., Cloern, J.E., Koseff, J.R., Monismith, S.G., Thompson, J.K.,

1998. Does the Sverdup critical depth model explain bloom dynamics in

estuaries? Journal of Marine Research 56 (2), 375e415.

Lucas, L.V., Koseff, J.R., Cloern, J.E., Monismith, S.G., Thompson, J.K.,

1999. Processes governing phytoplankton blooms in estuaries. I: The local

production-loss balance. Marine Ecology-Progress Series 187, 1e15.

Macintyre, H.L., Geider, R.J., Miller, D.C., 1996. Microphytobenthos: The

ecological role of the ‘‘Secret Garden’’ of unvegetated, shallow-water ma-

rine habitats: I. Distribution, abundance and primary production. Estuaries

19 (2A), 186e201.

May, C.L., Koseff, J.R., Lucas, L.V., Cloern, J.E., Schoellhamer, D.H., 2003.

Effects of spatial and temporal variability of turbidity on phytoplankton

blooms. Marine Ecology Progress Series 254, 111e128.

Mayer, L.M., Schick, L.L., Sawyer, T., Plante, C.J., Jumars, P.A., Self, R.L.,

1995. Bioavailable amino acids in sediments: A biomimetic, kinetics-

based approach. Limnology and Oceanography 40 (3), 511e520.

Middelboe, M., Kroer, N., Jorgensen, N.O.G., Pakulski, D., 1998. Influence of

sediment on pelagic carbon and nitrogen turnover in a shallow Danish es-

tuary. Aquatic Microbial Ecology 14 (1), 81e90.

Middelburg, J.J., Nieuwenhuize, J., 1998. Carbon and nitrogen stable isotopes

in suspended matter and sediments from the Schelde Estuary. Marine

Chemistry 60, 217e225.

Monbet, Y., 1991. Control of phytoplankton biomass in estuaries: A comparative

analysis of microtidal and macrotidal estuaries. Estuaries 15 (4), 563e571.

Murray, A.E., Hollibaugh, J.T., Orrego, C., 1996. Phylogenetic compositions

of bacterioplankton from two California estuaries compared by denaturing

gradient gel electrophoresis of 16S rDNA fragments. Applied and Environ-

mental Microbiology 62 (7), 2676e2680.

Murrell, M.C., 1999. Microbial processes and food web dynamics in a turbid

estuary: Northern San Francisco Bay, California, United States of America.

Ph.D. Dissertation., University of California, Santa Cruz, 169 pp.

Nichols, F.H., Thompson, J.K., 1985. Timescales of change in the San Fran-

cisco Bay benthos. Hydrobiologia 129 (1), 121e138.

Noji, T.T., Noji, C.I., Barthel, K.-G., 1993. Pelagic-benthic coupling during the

onset of winter in a northern Norwegian fjord: carbon flow and fate of sus-

pended particulate matter. Marine Ecology-Progress Series 93 (1e2),

89e99.

Odum, W.E., 1984. Dual-gradient concept of detritus transport and processing

in estuaries. Bulletin of Marine Science 35 (3), 510e521.

Powell, T.M., Cloern, J.E., Huzzey, L.M., 1989. Spatial and temporal variabil-

ity in South San Francisco Bay, California, USA I. Horizontal distributions

of salinity suspended sediments and phytoplankton biomass and productiv-

ity. Estuarine Coastal and Shelf Science 28 (6), 583e598.

Rhoads, D., 1974. Organism-sediment relations on the muddy sea floor.

Oceanography and Marine Biology: An Annual Review 12, 263e300.

Sagan, G., Thouzeau, G., 1998. Microphytobenthic biomass in the Bay of Brest

and the western English Channel. Oceanologica Acta 21 (5), 677e694.

Schafer, J., Blanc, G., Lapaquellerie, Y., Maillet, N., Maneux, E., Etcheber, H.,

2002. Ten-year observation of the Gironde tributary fluvial system: fluxes

of suspended matter, particulate organic carbon and cadmium. Marine

Chemistry 79, 229e242.

Schlacher, T.A., Wooldridge, T.H., 1996. Origin and trophic importance of de-

tritusdevidence from stable isotopes in the benthos of a small, temperate

estuary. Oecologia 106 (3), 382e388.

Schoellhamer, D.H., 1996. Factors affecting suspended-solids concentrations

in south San Francisco Bay, California. Journal of Geophysical Research.

C. Oceans 101 (C5), 12087e12095.

Sharp, J.H., Cifuentes, L.A., Coffin, R.B., Pennock, J.R., Wong, K.-C., 1986.

The influence of river variability on the circulation, chemistry, and micro-

biology of the Delaware Estuary. Estuaries 9, 261e269.

Smith, S.V., Hollibaugh, J.T., Dollar, S.J., Vink, S., 1989. Tomales Bay, Cal-

ifornia, USA: a case for carbon-controlled nitrogen cycling. Limnology

and Oceanography 34 (1), 37e52.

Sobczak, W., Cloern, J., Jassby, A., Mueller-Solger, A., 2002. Bioavailability

of organic matter in a highly disturbed estuary: the role of detrital and algal

resources. Proceedings of the National Academy of Sciences of the United

States of America 99 (12), 8101e8105.

Spiker, E.C., 1981. Stable carbon isotopes as a source indicator of organic car-

bon in estuaries. Estuaries 4 (3), 252.

Stribling, J.M., Cornwell, J.C., 1997. Identification of important primary pro-

ducers in a Chesapeake Bay tidal creek system using stable isotopes of car-

bon and sulfur. Estuaries 20, 77e85.

Thompson, J.K., Nichols, F.H., 1988. Food availability controls seasonal

cycle of growth in Macoma balthica (L.) in San Francisco Bay, California

USA. Journal of Experimental Marine Biology and Ecology 116 (1),

43e62.

Thompson, J.K., Nichols, F.H., Wienke, S.M., 1981. Distribution of benthic

chlorophyll in San Francisco Bay, California, February 1980eFebruary

1981. U.S. Geological Survey Open File Report 81e1134, Menlo Park,

CA, 36 pp.

Tietjen, J.H., 1968. Chlorophyll and pheo-pigments in estuarine sediments.

Limnology and Oceanography 13 (1), 189e192.

Turley, C.M., Hughes, D.J., 1992. Effects of storage on direct estimates of bac-

terial numbers of preserved seawater samples. Deep-Sea Research, Part A:

Oceanographic Research Papers 39 (3e4), 375e394.

Turley, C.M., Hughes, D.J., 1994. The effect of storage temperature on the

enumeration of epifluorescence-detectable bacterial cells in preserved

sea-water samples. Journal of the Marine Biological Association of the

United Kingdom 74 (1), 259e262.

USGS, 2003. San Francisco Bay Water Quality data. USGS, Menlo Park, CA.

http://sfbay.wr.usgs.gov/access/wqdata/index.html.

Van Duyl, F.C., Kop, A.J., 1990. Seasonal patterns of bacterial production and

biomass in intertidal sediments of the western Dutch Wadden Sea, Nether-

lands. Marine Ecology-Progress Series 59 (3), 249e262.

Velji, M.I., Albright, L.J., 1986. Microscopic enumeration of attached marine

bacteria of seawater marine sediment fecal matter and kelp blade samples

following pyrophosphate and ultrasound treatments. Canadian Journal of

Microbiology 32 (2), 121e126.

Velji, M.I., Albright, L.J., 1993. Improved sample preparation for enumeration

of aggregated aquatic substrate bacteria. In: Kemp, P.F., Sherr, B.F.,

Sherr, E.B., Cole, J.J. (Eds.), Handbook of Methods in Aquatic Microbial

Ecology. Lewis Publishers, Chelsea, MI, pp. 139e142.

Vidal, M., Morgui, J.-A., 2000. Close and delayed benthic-pelagic coupling in

coastal ecosystems: the role of physical constraints. Hydrobiologia 429

(1e3), 105e113.

Zimmerman, A.R., Canuel, E.A., 2001. Bulk organic matter and lipid bio-

marker composition of chesapeake bay surficial sediments as indicators

of environmental processes. Estuarine, Coastal and Shelf Science 53 (3),

319e341.

http://sfbay.wr.usgs.gov/access/wqdata/index.html

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