Estuaries Vol. 20, No. 2, p. 346-364 June 1997

Benthic Metabolism and Nutrient Cycling in Boston Harbor,

Massachusetts

ANNE E. GIBLIN’

CHARLES S. HOPKINSON

JANE TUCKER The Ecosystems Center Marine Biological Laboratory Woods Hole, Massachusetts, 02543

ABSTRACT: To gain insight into the importance of the benthos in carbon and nutrient budgets of Boston Harbor and surrounding bays, we measured sediment-water exchanges of oxygen, total carbon dioxide (DIC), nitrogen (ammonium, nitrate + nitrite, urea, N,O), silicate, and phosphorus at several stations in different sedimentary environments just prior to and subsequent to cessation of sewage sludge disposal in the harbor. The ratio of the average annual DIC release to 0, uptake at three primary stations ranged from 0.84 to 1.99. Annual average DIC:DIN flux ratios were consistently greater than predicted from the Redfield ratio, suggesting substantial losses of mineralized N. The pattern was less clear for P: some stations showed evidence that the sediments were a sink for P while others appeared to be a net source to the water column over the study period. In general, temporal and spatial patterns of respiration, nutrient fluxes, and flux ratios were not consistently related to measures of sediment oxidation-reduction status such as Eh or dissolved sulfide. Sediments from Boston Harbor metabolize a relatively high percentage (46%) of the organic matter inputs from phytoplankton production and allochtbonous inputs when compared to most estuarine systems. Nutrient regeneration from the benthos is equivalent to 40% of the N, 29% of the P, and more than 60% of the Si demand of the phytoplankton. However, the role of the benthos in supporthrg primary production at the present time may be minor as nutrient inputs from sewage and other sources exceed benthic fluxes of N and P by lo-fold and Si by 4fold. Our estimates of denitri- fication from DIC:DIN fluxes suggests that about 45% of the N mineralized in the sediments is denitrified, which accounts for about 17% of the N inputs from land.

Introduction Sediments of coastal environments play an im-

portant role in nutrient recycling and organic mat- ter decomposition (Nixon 1981; Boynton and Kemp 1985; Boynton et al. 1991). Many studies have focused on the role of the sediments in re- turning nutrients to the overlying water to support primary production and on the importance of the sediments in consuming oxygen from the water column (Zeitzschel 1980; Fisher et al. 1982; Garber 1987; Kemp and Boynton 1992).

Coastal sediments also serve as an important re- gional sink for nutrients. Nixon et al. (1976) ob- served that the ratio of oxygen uptake to inorganic nutrient release in sediments was higher than ex- pected from the decomposition of marine organic matter having a “Redfield” elemental stoichiome- tery of COs:N1s:P1 (Redfield 1934). Anomalously high 0:N ratios were attributed either to nitrogen lost as nitrogen gas via denitrification, or to an un- measured loss of N as dissolved organic nitrogen. Subsequently, the denitrification of mineralized N via coupled ammonification-nitrification-denitrifi-

1 Corresponding author. tele: (508) 289-7488; fax: (508) 457. 1548; e-mail: agiblin@lupine.mbl.edu.

0 1997 Estuarine Research Federation 346

cation was shown to be a major sink for N in es- tuarine sediments, generally removing 15-70% of the inorganic N mineralized from decomposing organic matter (Seitzinger 1988). The incomplete return of mineralized N from sediments is believed to be one of the factors contributing to the com- mon observation that N is the nutrient most lim- iting to primary production in coastal marine wa- ters (Ryther and Dunstan 1971; Nixon and Pilson 1983; Seitzinger et al. 1984). This removal of N in sediments also has a significant impact on the flow of nutrients from land to the coastal ocean. In an examination of the element budgets of nine estu- arine ecosystems of the North Atlantic, Nixon et al. (1996) concluded that 30-65010 of the N enter- ing the ecosystems was lost via denitrification or sequestered in sediments and not exported to the coastal ocean.

Phosphorus retention in estuaries can also be substantial. Of the nine systems examined by Nix- on et al. (1996), P retention ranged from 10% to 55% of the inputs for eight systems. In Chesapeake Bay, retention exceeded terrestrial inputs, imply- ing a net import of P from the coastal ocean. Phos- phorus is not lost in gaseous form, but mineralized P may be retained in sediments by adsorption or

Benthic Metabolism and Nutrient Cycling 347

authogenic mineral formation (Pomeroy et al. 1965; Patrick and Khalid 1974, reviewed in Ho- warth et al. 1995). Although some benthic flux studies have demonstrated that nearly all mineral- ized P is released to the overlying water (Nixon et al. 1976; Dollar et al. 1991)) others have found sub- stantially less P release than P mineralization, as estimated by measures of metabolism such as oxy- gen uptake (Smith et al. 1981; Nowicki and Nixon 1985). Less attention has been focused on P reten- tion in estuarine and coastal sediments because of the perceived importance of N as the nutrient lim- iting primary production (Ryther and Dunstan 1971). However, some estuaries and coastal marine systems may exhibit spatial or seasonal shifts in N versus P limitation of production (D’Elia et al. 1986). It has also been suggested that P limitation in temperate estuaries may have been more im- portant in the past when anthropogenic inputs and ratios of N to P were different (Howartb et al. 1995).

While silica is not limiting to overall primary production, decreases in the relative abundance of Si to N and P has the potential to alter the phy- toplankton community structure. Silica favors the production of diatoms (Officer and Ryther 1980; Ryther and Officer 1981; Doering et al. 1989). Be- cause anthropogenic inputs are frequently char- acterized by high N:Si ratios, the importance of Si as a control of community structure increases with eutrophication (Conley et al. 1993). This increase in Si control of community structure is potentially important as diatoms are believed to be the pre- ferred food of macro-grazers and a decrease in di- atoms may potentially lead to an increase in un- desirable toxic algal blooms (Smayda 1990; Conley et al. 1993).

To assess the response of estuaries and coastal systems to alterations in organic matter loading and nutrient inputs, it is necessary to understand what controls the magnitude and stoichiometric ra- tios of benthic fluxes. Benthic fluxes of oxygen, C, N, P, and Si respond to changes in the organic loading rate to the sediment (Hargrave 1973; Kemp and Boynton 1981; Nixon 1981; Kelly and Nixon 1984; however, the relative response of each element to changes in loading may be quite dif- ferent (Conley and Johnstone 1995). Increased or- ganic matter loading to sediments has been shown to decrease the percentage of N removed via de- nitrification (Seitzinger and Nixon 1985)) to de- crease P trapping within sediments (Howarth et al. 1995), to increase Si retention (Conley and John- stone 1995), and to increase the percent of the deposited organic carbon, which is eventually bur- ied (Henrichs and Reeburg 1987; Canfield 1989). Macrofaunal activity in sediments (Rhodes 1974;

Aller 1982; Banta 1992) is an additional factor that may alter the stoichiometery of benthic fluxes and change the efficiency with which C, N, P, and Si are released to the overlying water, sequestered in sediments, or removed via denitrification.

To gain insight into the controls on the magni- tude and elemental composition of benthic fluxes, we measured sediment-water exchanges of oxygen, total carbon dioxide (DIC), nitrogen, silicate, and phosphorus at several stations in Boston Harbor and surrounding bays. Measurements were made just prior to and subsequent to cessation of sludge disposal in the harbor. We measured fluxes for 3 yr at one station, where the sludge had been dumped for decades, to assess the relationship be- tween loading and benthic fluxes. Relatively few studies have examined benthic fluxes for more than 1 yr (Dollar et al. 1991; Boynton et al. 1995) or followed the response of benthic fluxes to changes in loading (Smith et al. 1981; Boynton et al. 1995). A number of other stations, less directly affected by sludge disposal, were also sampled.

Respiration was measured using both oxygen up- take and DIC release to determine the seasonal pattern and long-term storage of the reduced end- products of anaerobic metabolism. Urea and ni- trous oxide, two components of nitrogen flux that are not frequently measured, were included to de- termine their importance in the overall N budget of the sediments of Boston Harbor.

Station Location and Description Three primary stations within Boston Harbor

and Hingham Bay were sampled one to five times a year from September 1991 to October 1994 (Fig. 1; Table 1). The stations sampled ranged from or- ganic-rich, fine-grained sediments to hard sand and gravel and were chosen to reflect the various sedimentary environments of Boston Harbor. The majority (51%) of the harbor is classified as de- positional, 20% is erosional or nondepositional, and the remainder of the harbor is classified as strongly reworked (Knebel and Circe 1995). An- nual cycles ‘(4 to 5 samplings per year) were ob- tained at station BH03 in 1992, 1993, and 1994; at BH02 in 1993 and 1994; and at BHOS in 1992. Sta- tion BH03 is located in a depositional area off Long Island. Sewage sludge was dumped in this area until January 1992. Sediments are fine grained and flocculent. Station BH02 is in an area of sediment reworking located on Governors Is- land Flats. The sediments are largely composed of fine-grained muds. Station BHOS is in an erosional area of Hingham Bay where sediments are primar- ily sands with some small gravel. There was a dense sand-shell-gravel layer at S-10 cm depth at this site.

Three additional stations were sampled to better

348 A. E. Giblin et al

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TABLE 1. Stations for flux studies.

Nominal Depth Site

Station (m) Description %C %N

BH02 12 -55% silt-clay 0.52-3.42 0.06-0.44 BH03 7 >50% silt-clay 2.70-4.46 0.32-0.53 BH07 6 -55% sand 2.81-3.64 0.35-0.45 BH08 13 >80% sand and 0.14-0.38 0.03-0.05

gravel T4 3.5 -63% silt-clay 3.88-6.06 0.39-0.80 R4 5.5 -55% sand 1.82 0.19

assess spatial variability in the Boston Harbor re- gion. Station BH07 was sampled in September 1991, August 1992, and July 1994. The station is located in a depositional area in Quincy Bay. Sed- iments from this station are fine grained but con- tain more sand than station BH03. Two additional stations, R4 and T4, were sampled once in August 1992. Stations R4 and T4 are located in deposi- tional areas of Boston Harbor. Sediments at station T4 consist predominately of fine-grained muds, sediments at station R4 contained more sand.

Further descriptions of sediment parameters and benthic infauna can be found in Blake et al. (1993), Kelly and Kropp (1992), and Kropp and Diaz (1995).

Methods

SAMPLING

Stations were located using a differential global positioning system provided by Battelle Ocean Sci- ence (Duxbury, Massachusetts). Station locations using this system should be accurate within 10 m.

All stations were sampled by SCUBA divers. At each station several sizes of sediment cores were taken. Two to three large 15-cm diameter core tubes were used to obtain sediment for flux mea- surements. Replicate 6.5-cm diameter core tubes were used to obtain sediment for porewater anal- ysis and Eh measurements. Three to four 2.5-cm diameter cores were taken for porosity and solid phase analyses.

Bottom water temperature at all stations was de- termined by measuring the temperature of the wa- ter taken near the bottom with a Niskin bottle. Sa- linity was measured using a refractometer.

At each station 15 1 of water were collected with a diaphragm pump from just above the bottom and filtered immediately through a series of car- tridge filters (nominally 20 l..r,rn and 1.0 Frn). This water, which was held at in situ temperatures, was

Benthic Metabolism and Nutrient Cycling 349

used to replace the water overlying the cores used for flux measurements.

BENTHIC RESPIRATION AND NUTRIENT FLUXES

Cores were transported to Woods Hole and placed in a dark incubator where they were held uncapped, overnight, at the in situ temperature of the station. Flux measurements were begun within 12-48 hours of sampling. Prior to initiating flux measurements, the overlying water of each core was replaced with the filtered seawater obtained from each station. Two 300-ml BOD bottles filled’ with the filtered water obtained from each station were used to measure the changes in oxygen and nutrients of the water overlying the sediments. Two 60-ml BOD bottles were filled with filtered water and used to measure changes in total dissolved in- organic carbon (DIG) in the water.

Benthic flux measurements were made accord- ing to the protocols described in Banta et al. (1995). Cores were sealed with core tops contain- ing magnetic stirrers (Dornblaser et al. 1989) and gently mixed. Using an oxygen electrode, we mon- itored concentrations of oxygen in the overlying water every l-4 h throughout the incubation pe- riod. DIC was measured at the beginning and end of the incubation. Incubation duration was deter- mined by the time required for oxygen concentra- tions to fall by 2 ppm to 5 ppm (generally 6 h to 48 h). Benthic respiration was calculated from the change in the oxygen and DIC concentration ver- sus time. If necessary the values were corrected for the oxygen uptake in the water overlying the cores by using O2 or DIC changes measured in BOD bot- tles, but for most of the incubations, water column respiration was negligible.

Concurrent with 0, measurements, samples of the overlying water were withdrawn for dissolved inorganic nutrients at least four times over the in- cubation period. Ammonium concentration was determined immediately from duplicate 3-ml sub- samples by the technique of Solorzano (1969) modified for small sample size. A 2-ml sample was saved for phosphate analysis; it was acidified to pH 2 with 10 l.r,l of 4.8 N HCI and kept at 4°C until analysis. Samples were analyzed using the spectro- photometric method of Murphy and Riley (1962). Additional water was frozen for later measurement of the nitrate + nitrite, silicate, and urea concen- trations. Nitrate + nitrite was determined together using the cadmium reduction method on a rapid

t

Fig. 1. a) A map of the station locations sampled in this study. b) The water temperature at each station at the time it was sampled for benthic fluxes.

350 A. E. Giblin et al

flow analyzer (Alpkem RFA-300). DIN was calcu- lated as the sum of ammonium, nitrate, and nitrite.

In 1993 and 1994, silicate was analyzed by re- duction with stannous chloride using an autoana- lyzer (method of Armstrong 1951 as adapted by RFA, Alpkem Corporation 1986). Urea was ana- lyzed using the method of Price et al (Price and Harrison 1987). In 1993 we experienced problems with urea contamination in the samples. We dis- covered that the vials being used for sample stor- age (standard scintillation vials) had caps made of polyurea and these breakdown during the acid- washing of the vials.

At the beginning of the incubation period and after 24 h, samples of overlying water were taken for N,O analysis. Duplicate 15-ml samples were taken from two cores from each station using a gas- tight syringe. Metabolic activity was stopped by the addition of sulfuric acid to bring the pH down to 1. N,O was analyzed within 24 h. The water sam- ples were equilibrated with a N2 headspace, and analyzed with a Shimadzu gas chromatograph equipped with an electron capture detector.

DIC samples were preserved with mercuric chlo- ride and stored at 4°C. Samples were analyzed with a high precision coulometric CO, analyzer (John- son et al. 1993). The instrument is capable of mea- suring total CO, with a precision of 0.05% (1 Frn) .

POREWATER SAMPLING AND ANALYSIS

Sediment samples for porewater extraction were sectioned into depth intervals inside a glove bag under a nitrogen atmosphere. Sediments were nor- mally sampled in l-cm intervals down to 2 cm, 2-cm intervals to 10 cm, and then in 4cm intervals at greater depths. Porewater was removed from muddy sediments by centrifuging sections of mud for 15 min in centrifuge tubes capped under nitro- gen. Sediments at station BHOS were very sandy. Here it was necessary to use a “split” centrifuge tube. A filter support with filter (GF/F) is placed midway down the tube and sediments are placed on top of the filter. Centrifuging at high speed for 15 min forces porewater through the filter into the bottom of the tube.

Porewater was subsampled immediately for nu- trients, sulfides, pH, and alkalinity after centrifu- gation. Nutrients were analyzed as described above. Samples for sulfide analysis were immedi- ately fixed in 2% zinc acetate and analyzed within 12 h using the method of Cline (1969). Samples for pH and alkalinity were analyzed immediately. Alkalinity was analyzed using a Gran titration (Ed- mond 1970).

Sediment redox potential was measured on a separate sediment core using a platinum electrode (Bohn 1971). The electrode was pushed into the

sediment at 1.0 to 3.0 cm increments and allowed to stabilize for 15 min. The resulting EMF was read on a standard pH meter connected to a saturated calomel reference electrode placed in the overly- ing water. The calibration of the electrode was checked by measuring the EMF of quinhydrone dissolved in buffers of pH 4 and 7 (Bohn 1971). The values reported here have been corrected for the potential of the reference electrode. Before be- ginning the Eh measurements the depth of the re- dox potential discontinuity was visually estimated by the depth of color change in the sediment and qualitative notes on animal burrows were made.

SEDIMENT C AND N

Organic carbon and nitrogen analyses were per- formed on the O-2 cm section of the sediments using a Perkin Elmer 2400 CHN elemental analyz- er. Sediments were placed in a desiccator over fum- ing HCl to remove any carbonates that might have been present (Kristensen and Andersen 1987). The percent carbon and percent nitrogen mea- sured on the sediment was corrected for the weight change due to the procedure.

Results and Discussion

SEDIMENT PARAMETERS

Sediments from depositional areas had the high- est carbon and nitrogen contents (Table 1). Sta- tion BHOS, which is in an erosional area, had very low C contents, ranging from 0.14% to 0.38% dur- ing the study period. The carbon content at station BH02 was between that of most of the depositional stations. Carbon content at station BH02 showed large temporal variations but did not exhibit sea- sonal or long-term trends. Station BH02 is located in an area of intense sediment reworking, which may account for the variability.

SEDIMENT RESPIRATION

Sediment oxygen uptake ranged from approxi- mately 7 mmol 0, m-* d-l to 220 mmol 0, mm2 d-l. For 12 of the 15 samplings, the highest oxygen uptake rates were measured at station BH03, the former sludge disposal site (Fig. 2). When aver- aged over an annual cycle, the oxygen uptake rates at station BH03 exceeded those measured at BH02 and BH08 in every year. Oxygen uptake at stations T4, R4, and T7 ranged from 22 0, mm2 d-l to 45 mmol O2 me2 d-l and were usually within 20% of the rates measured at BH02 at the same time (data not shown, Giblin et al. 1992, 1993, 1995).

The sludge disposal site, BH03, also exhibited the highest interannual variability in oxygen up- take. The average annual oxygen consumption measured in 1993 (133 mmol 0, mm2 d-l) was more than twice what we measured in 1992 or 1994

Benthic Metabolism and Nutrient Cycling 351

250, Sediment Respiration

9 3 4 5 6 7 6 9 1011 3 4 5 6 7 6 9 1011 3 4 5 6 7 8 9 1011

250,

,GG 200

-I

BH02

“E

9 3 4 5 6 7 6 9 1011 3 4 5 6 7 6 9 1011 3 4 5 6 7 6 9 1011

120 -

-; 100 ~~ BH08 oi E 80 ~- 5 5 60-- N

8 40.- T T

9 3 4 5 6 7 6 9 1011 3 4 5 6 7 6 9 1011 3 4 5 6 7 8 9 1011 1991 1992 Month and Year 1993 1994

Fig. 2. The average rates of oxygen uptake and DIC release of sediments from the three primary stations (mean + SE n = 2 or 3).

(50 mmol 0, me2 d-l) These very high sediment oxygen uptake rates occurred more than a year after sludge disposal had ceased. The high 1993 oxygen uptake rates exceeded almost all rates re- ported in the literature from natural systems and were slightly higher than rates measured in highly nutrient-loaded experimental mesocosms (Sam- pou and Oviatt 1991). Rates measured at station BH03 in September 1991, when disposal was still taking place, were lower than rates measured dur- ing similar times of the year in the subsequent 3 yr. The September 1991 measurements were made shortly after a hurricane passed through the region and possibly not representative of the average pre- disposal condition (Giblin et al. 1992).

Respiration at BH08, the sandiest station, was consistently low, ranging from 7 mmol 0, m-* d-l

in winter to 24-28 mmol 0, m-* d-l in summer. The average annual rate was 20 mmol 0s mm2 d-l. These rates are quite low and are representative of coastal areas with low nutrient inputs such as Buz- zards Bay, Massachusetts (Banta et al. 1995). Sta- tion BHOS was only sampled over an annual cycle in 1992, but summer oxygen uptake rates in 1991- 1994 were similar, suggesting that interannual vari- ation in respiration at this station is low.

Oxygen uptake at BH02 ranged between 20 mmol mm2 d-l 30 mmol mm2 d-l in the autumn and winter and reached values of 50-100 mmol m-* d-l in the spring and summer. Oxygen uptake rates usually fell between those measured at BH03 and BH08. These rates are fairly typical of values reported for estuaries receiving moderate to high inputs of nutrients such as Chesapeake Bay (Boyn-

352 A. E. Giblin et al

ton and Kemp 1985), the Neuse River estuary (Fisher et al. 1982), and productive coastal areas such as the Georgia Bight (Hopkinson 1987). Ox- ygen uptake rates measured in the same month of the different years were fairly similar to each other with two exceptions; in May 1993 oxygen uptake was twice as rapid as it was in 1994, and in Septem- ber of 1991 it was low when compared to late sum- mer and early autumn rates in subsequent years. The average annual rate of oxygen uptake in 1993 (53 mmol 0, m-2 d-l), was higher than the rate measured in 1994 (33 mmol 0, me2 d-l).

Total DIC release ranged from 10 mmol mm2 d-l to 185 mmol m-* d-l (Fig. 2). The seasonal pattern of DIC fluxes was fairly similar to oxygen uptake at all three stations. From 1991 to 1993 the highest DIC release rates were usually observed at station BH03. DIC release averaged over an annual cycle at BH03 in 1992 (57 mmol C m-2 d-l) and 1993 (111 mmol m-* d-l) exceeded rates measured at the other stations. In 1994 rates averaged over an annual cycle were slightly higher at BH02 (66 mmol C mm2 d-l) than at BH03 (61 mmol C m-* d-l). DIC release at BH02 showed less interannual variation than oxygen uptake. Average rates at this station in 1993 (74 mmol C mm2 d-l) were only slightly higher than in 1994. BHOB had the lowest annual DIC release rate (24 mmol m-* d-l).

NITROGEN FLUXES

The combined flux of DIN (ammonium + ni- trate + nitrite) across the sediment-water interface ranged from a slight uptake of 0.03 mmol N m-* d-l at station BH03 in March 1994 to a release of more than 20 mmol N m-* d-l at station BH03 in July 1993 (Fig. 3). The general seasonal pattern of DIN fluxes roughly followed the pattern of sedi- ment respiration, and the large interannual varia- tion noted in respiration at station BH03 was also evident in the DIN fluxes. Differences between sta- tions were also similar to that of oxygen uptake with the highest DIN fluxes usually being observed at station BH03 and the lowest at station BHOB. Intermediate rates were measured at the other sta- tions.

The relative contribution of ammonium and ni- trate to the DIN flux showed marked differences between stations and marked seasonal and annual differences (Fig. 3). Nitrate was consistently im- portant at station BHOB making up 15-80% of the total DIN flux. Nitrate was usually not an impor- tant component of the DIN flux at station BHOZ. During the spring and winter, nitrate was some- times taken up; however, during the October sam- plings of 1993 and 1994 nitrate efflux was impor- tant, making up about 40% of the DIN flux. Ni-

trate fluxes at station BH03 ranged from 0% of the DIN (March 1994 when nitrate was taken up) to 100% of the DIN efflux. In 1993 nitrate efflux ex- ceeded ammonium efflux and in 1992 and 1994 nitrate efflux made up about 30% of the annual DIN flux. In the three summer and autumn mea- surements made at station BH07, nitrate composed 14-18% of the DIN flux. In the single August sam- pling made at stations R4 and T4, sediments took up nitrate from the overlying water column.

Urea is a nitrogenous compound excreted by some macrofauna. In some areas urea makes a very substantial contribution to the N flux from sedi- ments (Lomstein et al. 1989). Because it has an exceedingly low C:N ratio (0.5) and is readily bro- ken down in the water column to inorganic nitro- gen, urea fluxes must be considered when calcu- lating flux stoichiometery and N budgets.

The fluxes of the urea we measured were small in comparison to DIN fluxes. Urea fluxes from all stations ranged from -0.03 mmol mm2 d-l to a maximum of 0.14 mmol m-* d-l. The r* values for the majority of the regressions of concentration against time were low and in most cases not signif- icantly different from zero.

N,O fluxes were also exceedingly small in com- parison to DIN fluxes. In a number of cases N,O fluxes were negative. Fluxes averaged less than 10 pmol m-* d-l and never exceeded 20 pmol m-* d-l.

PHOSPHATE FLUX

Phosphate fluxes ranged from an uptake of -0.4 mmol mm2 d-l to a release of 7.8 mmol m-* d-l (Fig. 4). Phosphate fluxes did not exhibit seasonal or spatial patterns that were similar to either sed- iment respiration or nitrogen fluxes. For example, phosphate fluxes in 1992 were slightly higher at the sandy station BHOB (0.32 mmol m-* d-l) than at the sludge disposal site, BH03 (0.25 mmol mm2 d-l), and in 1993, phosphate fluxes at BH02 (1.97 mmol mm2 d-l) were much greater than at BH03 (0.77 mol m-* d-l). Sediment respiration at BH03, however, exceeded that of either station by more than twofold in both years. The average phosphate fluxes we observed at both BH02 (0.41 mmol mm2 d-l) and BH03 (0.07 mmol m-* d-l) were lower in 1994 than we observed in 1993 and the seasonal pattern was also different. In both years, DIP fluxes were higher at station BH02 than at BH03.

SILICA FLUXES

There was a large interannual variation in Si fluxes at both station BH03 and BH02 (Fig. 5). Average Si fluxes at station BH03 were three times greater in 1993 (18.3 mmol m-* d-l) than in 1994 (4.9 umol mm2 d-l). In contrast, Si fluxes at station

Benthic Metabolism and Nutrient Cycling 353

DIN Flux 25.00 , I

“_.,U

9 3 4 5 6 7 8 9 1011 3 4 5 6 7 8 9 1011 3 4 5 6 7 8 9 1011

-5.00 1 I

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-I 91991 3 4 5 6,$gj 9 1011 3 4 5 6 7 qg&lo 11 3 4 5 6 Tg&9 1011

Month and Year

Fig. 3. The average benthic fluxes of dissolved inorganic nitrogen of sediments from the three primary stations (mean + SE n = 2 or 3). Ammonium and nitrate fluxes have been separated to show the relative importance of the different DIN species.

BH02 were higher in 1994 (8.2 mmol m-* d-l) than in 1993 (5.6 mmol mm2 d-l). Silica flux rates measured at the sandy BH08 station were always lower than the rates measured at other stations at the same time. In general, Si fluxes had a seasonal pattern similar to sediment respiration and DIN fluxes.

POREWATER CONSTITUENTS AND EH

Although there were large seasonal and inter- annual changes in most of the porewater constit- uents, there were some very consistent station to station differences (Fig. 6). At station BH08, the sandiest station, we almost never detected dis- solved sulfide in the porewater, alkalinity values

usually ranged from 2.5 to 4.5 mEq, and nitrate could be routinely detected to depths of 5 cm. Dis- solved ammonium concentrations in the porewater rarely exceeded 0.5 mM and dissolved phosphate concentrations almost never exceeded 100 uM.

In contrast to the sandy BH08 station, dissolved sulfide concentrations in the sediments from all other stations commonly reached values of 0.5-7 mM at depth. Nitrate was rarely detected in the porewater and never exceeded 2 uM. Dissolved ammonium concentrations consistently reached 0.5-3 mM below 10 cm and alkalinity values com- monly ranged from 5 mEq to 40 mEq at depth (Fig. 6).

There were seasonal changes in all porewater pa-

354 A. E. Giblin et al.

3 DIP Flux

9 3 4 5 6 7 8 9 1011 3 4 5 6 7 8 9 1011 3 4 5 6 7 6 9 1011

-1 9 3 4 5 6 7 8 9 1011 3 4 5 6 7 6 9 1011 3 4 5 6 7 8 9 1011

-1

&I 3 4 5 6 1992 7 8 9 1011 3 4 5 6 7 8 9 1011 3 4 5 6 7 8 9 1011

Month and Year lgg3 1994

Fig. 4. The average benthic flux of dissolved inorganic phosphate from sediments from the three primary stations (mean + SE n=2or3).

rameters, although they did not always follow the expected relationships to sediment respiration or temperature. For example, there was a tendency for the top several centimeters of the sediment to be less reducing in summer in spite of much high- er rates of sediment metabolism (Fig. 6), and con- centrations of many porewater constituents were higher in early spring than in summer. Year to year changes in sediment Eh and sulfide concentrations at station BH03 also followed an inverse pattern to that of sediment respiration. In spite of much high- er respiration rates in 1993 compared to 1992 and 1994, sediment Eh values were higher in 1993 (Fig. 6).

Seasonal and interannual variations in apparent

redox potential discontinuity (RED), Eh, and dis- solved sulfide (Fig. 7) appeared to be related to visual observations of animal abundances made by divers during the sampling. For example, at station BH03 fairly low numbers of animals were observed in September 1991 and through the summer of 1992, after dumping ceased, until November 1992 when a large population of benthic amphipods was first observed. Amphipods were very abundant in the summer of 1993 and correspondingly, the RPD was deeper than in 1992 and concentrations of sul- fide in the top 8 cm were usually below detection. Abundances in the summer of 1994 appeared to be lower than in 1993 and there was a correspond- ing shallowing of the RPD. In November 1994

35

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0

-5

BH03

3 4 5 6 7 8 9 10 11 3 4 5 6 7 8 9 10 1,

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3 4 5 6 7 8 9 ,011 3 4 5 6 7 8 9 101

10

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3 4 5 6 7 8 9 ,011 3 4 5 6 7 8 9 1011 1993 Month and Year 1994

Fig. 5. The average flux of dissolved silica of sediments from the three primary stations (mean + SE n = 2). Silica measure- ments were only made in 1993 and 1994.

there was another increase in animal abundances, a deepening of the RPD, and a decrease in dis- solved sulfide in the top 8 cm. In contrast, at sta- tion BH02, animal numbers appeared to be low throughout 1993. No surface dwelling animals were observed in May 1993 when the RPD was at the surface, dissolved sulfide could be detected to the top cm, and a mat of white sulfur bacteria cov- ered the surface. Somewhat greater animal abun- dances were observed at BH02 in 1994, and there was a concomitant increase in RPD and a decrease in surface sulfide concentrations.

Our observations on animal abundances by di- vers were ‘qualitative but are supported by quanti- tative benthic animal samples taken twice a year at these stations by other investigators (Kropp and Diaz 1995; Fig. 7). For example, highest animal abundances at station BH03 were reported in Au- gust 1993 (350,000 individuals m-l, Kropp and Diaz 1995) at the same time we observed very high

Benthic Metabolism and Nutrient Cycling 355

numbers of infauna. Very few animals were ob- served in April 1993 at BH02 (Kropp and Diaz 1995) just before we observed reducing conditions at the sediment surface.

FIUX Ratios Most studies of benthic fluxes in estuarine and

coastal marine sediments have used oxygen as a measure of organic matter decomposition (Nixon et al. 1976; Boynton and Kemp 1985; Hopkinson 1987; Banta et al. 1995). The aerobic respiration of organic material with a composition similar to phytoplankton should produce 0.85-l mole of CO, for every mole of oxygen consumed (i.e., a respiratory quotient, RQ of 0.85 to 1). Although much of the organic matter in coastal sediments is decomposed through anoxic pathways, over an an- nual cycle, oxygen uptake should be a good proxy for total organic matter decomposition if most of the reduced endproducts of anoxic decomposi- tion, primarily sulfide, are oxidized.

In our study, the ratio of DIC release to oxygen uptake (RQ) ranged from 0.44 to 3.48, with the majority of values falling between 0.9 and 1.4 (Fig. 8). A regression of DIC versus 0, for the entire dataset (forced through zero) gives a slope of 0.97 (r* = 0.59), but individual stations behaved quite differently. For example, DIC release nearly always exceeded oxygen uptake at stations BH08 and BH02 (Table 2). In 1992, the annual average RQ at station BHOS was 1.19. The annual average RQ at station BH02 was 1.41 in 1993 and 1.99 in 1994. Annual average fluxes of DIC exceeded oxygen up- take at the sludge disposal site, BH03, in 1992 (RQ = 1.14) and in 1994 (RQ = 1.40). In 1993 oxygen uptake exceeded DIC release (RQ = 0.84), sug- gesting a net oxidation of sulfides in 1993 and a net storage in 1992 and 1994. This pattern corre- sponded to greater animal abundances and lower dissolved porewater sulfides in 1993.

In many estuarine and coastal marine environ- ments the burial of reduced sulfur is fairly small (Jorgensen 1982; Mackin and Swider 1989), but in sediments with high sedimentation rates (Chanton et al. 1987) it can be very high, leading to substan- tial discrepancies between oxygen uptake and or- ganic matter mineralization. Greater sulfur storage in sediments from station BH02 would be consis- tent with the more reduced nature of the sedi- ments when compared to those at stations BH03 or BH08. The large interannual variation in RQ values measured at BH03 also correspond to dif- ferences in sediment redox status and/or bio-irri- gation rates. RQ values were lowest in 1993 when animal abundances were high and near-surface sul- fide concentrations were at their lowest values.

Only a few studies have directly compared sedi-

356 A. E. Giblin et al.

Eh (mV) HS- (mM) Alk (mEq) NH4(mM) P04(uM) Si (uM)

Y

I

16.

800 1200

Fig. 6. Sediment Eh and porewater profiles from the three primary stations taken in March 1993, July 1993, and July 1994. These profiles were chosen to illustrate seasonable variability (March 1993 versus July 1993) and annual variability (July 1993 versus July i994). See text for details.

,

ment-water oxygen fluxes to the flux of total dis- solved inorganic carbon. Dollar et al. (1991) found a significant difference between the two measure- ments with nearly l/3 of the total sediment respi- ration that was not accounted for by oxygen being attributable to sulfate reduction. In Galveston Bay, upper bay sediments had a mean DIC:O, ratio of 0.96, indicating very little reduced sulfur storage, while lower bay sediments displayed a much higher ratio, 1.7 (Zimmerman and Benner 1994). It ap- pears that oxygen uptake may approximate total decomposition very closely in some systems and substantially underestimate it in others.

The ratio of DIC flux to DIN flux varied by an order of magnitude for individual stations and dates, but only on three occasions were the ratios of DIC to DIN lower than 6.625, the ratio that would be predicted from .the decomposition of or- ganic matter with a “Redfield composition” (Fig. 8). The DIC:DIN flux ratio of our entire dataset is

9.5 (r* = 0.65). DIC:DIN fluxes were highest in late winter-early spring and lowest in midsummer (data not shown). Average annual ratios ranged from a low of 9.6, measured at BH03 in 1993, to a high of 15.5, measured at BH03 in 1994 (Table 2).

The relationship between DIC and DIP fluxes was extremely variable. While for the majority of the observations, DIP release was less than pre- dicted from a Redfield C:P ratio of 106:1, extreme- ly low DIC:DIP ratios were observed at both sta- tions BHOZ and BHOS on one ocassion (Fig. 8). Because these low ratios occurred when overall fluxes were quite high, the average annual DIC: DIP flux ratios at these two stations were below 106 (Table 2). In contrast, the average annual DIC:DIP flux ratio at station BH03 was quite high, ranging from 145 to 943.

Large differences in the DIC:DIP flux ratios be- tween stations are reflected in the N:P flux ratios. The average annual flux ratios of DIN to DIP were

Benthic Metabolism and Nutrient Cycling

Sediment Redox and Animal Abundance

BH03

Fig. 7. Two measures of sediment redox status: the apparent redox potential discontinuity (RPD), determined visually; and the first depth in the sediments where porewater sulfides exceeded 10 UM in sediments from two of the primary stations. No data are shown for the third primary station, BHOS, because the apparent RF’D was not reliably visible and sulfides were rarely detected. The numbers of animals measured by Kropp and Diaz (1995) in September 1991 and April and August of 1992, 1993, and 1994 are shown for comparison. Animal samples were taken on separate cruises and at separate times from the flux cores but are in agreement with observations made during the flux cruises (see text for details). Station locations are the same within the limits of the navigation system.

less than 15 at BH02 and BHOS, indicating that the sediments were preferentially releasing P relative to N. In contrast, the DIN:DIP flux ratios at station BH03 ranged from 15 to 61, suggesting that the sediments were retaining P even more strongly than N.

Assuming that the majority of the organic matter decomposed is settled phytoplankton with a Red- field elemental composition and that DIC accu- rately reflects decomposition, we calculate from the high DIC:DIN fluxes that 31-57% of the nitro-

gen mineralized in sediments at all stations is not released to the overlying water (Table 2). Calcula- tions based upon DIN:DIP fluxes give a substan- tially different picture of DIN losses. The high DIN:DIP flux ratios we observed at station BH03 would lead us to conclude that all mineralized N is released at the sludge disposal station. In con- trast low N:P ratios at BH02 and BH08 would in- dicate that 28% to 78% of the remineralized N is not returned to the overlying water.

Denitrification was measured using direct N,

I 358 A. E. Giblin et al.

DIC vs DIN -200

‘; P

YE 150

5 EIOO

.c.

g 50

0

0 50 100 150 200 250

O2 (mmol~m~2d’ ) DIN (mmol.me2.d-’ )

n BH02 v BH03 A BH07 0 BH08 0 R4 A T4 n BH02 v BH03 a BH07 0 BH08 0 R4 a T4

DIN vs DIP

DIP (mmol~m~2 .d” ) -1

EIP (mmol~m~2~&’ ) 2

- BH02 7 BH03 A BH07 - BH08 0 R4 n T4 - BH02 v BH03 a BH07 - BH08 0 R4 a T4

DIC vs Si 200 40

I 6 ‘;

u

?E150

v B N’ 30

E ‘i5 I z El00 -- v E20 5 I

I v g g 50 -- -+ v A

77 l¶v = ZlO cl

* n m 07 I r : : I I : ! I 0 -10 0 10 20 30 40 -10 0 30 40

Si (mmol~m”.d~’ ) Si’(kmol+r?.de’

)

- BH02 v BH03 A BH07 - BH08 - BH02 v BH03 . BH07 = BH08

Fig. 8. The ratio of DIC versus O,, DIC versus DIN, DIC versus DIP, DIN versus DIP, DIC versus Si, and DIN versus Si for all sampling dates and stations. Each point represents the average value of the fluxes for a station at a sampling time. Lines show the values expected from the Redfield ratio (Redfield 1934, Redfield et al. 1963).

Benthic Metabolism and Nutrient Cycling 359

TABLE .2. Ratio of average benthic fluxes from the three primary stations. Ratios were calculated by taking the ratio of the average of each flux for the months sampled. Data is shown both with and without all the months sampled at station BH03 to allow for a direct comparison with the other stations that were sampled less frequently.

Year Months

Sampled Station DIC:O,

1992 4,5,6,8,11 BH03 1.14 4,5,6,8 BH03 1.16 425,628 BH08 1.19

1993 3, 5, 7, 8, 10 BH03 0.84 3, 5, 7, 8, 10 BH02 1.41 3, 5, 7, 10 BH03 0.82 3, 5, 7, 10 BH02 1.40

1994 3, 5, 7, 10 BH03 1.24 3, 5, 7, 10 BH02 1.99

DIC:DIN DIC:DIP

11.86 232.39 10.79 194.52 13.39 74.59

9.57 144.82 11.57 37.77

9.16 168.53 13.15 33.81

15.51 942.81 15.12 162.72

DIN:!3 DIC:Si DINDIP NO,:DIN Missing

N1

na na 19.60 0.31 44 na na 18.03 0.16 39 na na 5.57 0.38 51

0.64 6.09 15.13 0.62 31 1.15 13.32 3.27 0.05 43

0.76 6.93 18.40 0.60 28 1.15 15.10 2.57 0.01 50

0.80 12.39 60.77 0.31 57 0.53 8.05 10.77 0.11 56

1 %, Missing N = annual average (observed DIN flux/expected DIN fltrx)*lOO. The expected DIN flux was calculated from the annual average DIC flux assuming a Redfield C:N ratio of 6.625. See text for details.

flux measurements contemporaneously with our flux study (Kelly and Nowicki 1992, 1993; Nowicki 1994; Giblin et al. 1995). In general, the annual estimate of missing N made from the DIC:DIN stoi- chiometric relationships is in agreement with the direct measurements of denitrification. Differ- ences between the two methods ranged from less than 5% in 1993 to 40% in 1994 (Giblin et al. 1993; Giblin et al. 1994). The calculations based on DIC:DIN fluxes are in much better agreement with the direct measurements of denitrification than the DIN:DIP flux ratios. This suggests that DIP flux is not an accurate measure of decompo- sition in this system.

An alternative explanation for the anomalous flux ratios is that the organic matter decomposed in harbor sediments has a C:N:P stoichiometery that differs from the Redfield ratio. Surface sedi- ment C:N ratios at all stations generally ranged from 8-12. These values are typical of marine sed- iments (c.f. Zimmerman and Benner 1994; Banta et al. 1995). Studies have found C:N ratios of re- mineralized organic matter in surface sediments ranging from 5.5 to 6.6, substantially lower than ratios in bulk sediment (Burdige 1991; Zimmer- man and Benner 1994; LaMontagne 1995). The close agreement between C and N mineralized in sediments and the Redfield ratio suggest that our C:N assumption is probably reasonable.

Silica fluxes are influenced by the proportion of the organic matter derived from siliceous phyto- plankton. As this proportion varies substantially, Si release may not be well correlated with DIC pro- duction or N release. However, we did find a weak correlation between DIC and Si fluxes (r* = 0.50) and a stronger relationship between DIN and Si (r* = 0.69). Diatoms have a DIN:Si requirement of about 1 (Redfield et al. 1963). Most of the flux measurements have a DIN:Si ratio near or below

1, indicating that benthic fluxes in Boston Harbor are providing nutrients in a ratio favorable for di- atoms. The overall ratio of DIN:Si in the benthic fluxes is 0.46 (r2 = 0.69). The average annual ra- tios for station BH03 and BH02 ranged from 0.64 to 1.15 (Table 2).

Controls on Benthic Fluxes

RELATIONSHIP OF FLUXES TO TEMPERATURE

Correlations between respiration and tempera- ture differed from station to station. Whereas tem- perature explained most of seasonal variations in the oxygen and DIC fluxes at BH08, the sandy sta- tion (0, versus temperature, r2 = 0.90; 0s versus DIC, r2 = 0.73), correlations were low at station BH03 (r2 = 0.32) and BH02 (r2 = 0.14). When data for individual stations were combined there was no significant correlation between tempera- ture and respiration (Fig. 9).

As was the case for sediment respiration, corre- lations with temperature did not explain much of the variation in nutrient fluxes in the complete da- taset. At individual stations, temperature account- ed for 30% (station BH02). to 46% (at BH03) of the variation in DIN fluxes and from less than 1% (stations BH02) to 39% (at station BH03) of the variation in P fluxes. Temperature explains more than half of the variation in Si flux at BH08 (r2 = 0.6) and BH03 ( r2 = 0.58) but only 23% of the variance in the Si flux at BH02 (r2 = 0.23) (Fig. 9).

RELATIONSHIP OF FLUXES TO LOADING, BENTHIC MACROFAUNA AND SEDIMENT REDOX

It is normally assumed that increased organic loading to the sediments increases sediment me- tabolism (Hargrave 1973) and that increased sed- iment metabolism will lead to decreased oxygen penetration into the sediments and decreased sed-

360 A. E. Giblin et al.

O2 Flux vs Temp (a) 1993-l 994

p 200

;150

EIOO .z

6 50

0 0 5 10 15 20

Temp (“C)

n BH02 v BH03 A BH07 e BH08 0 R4 a T4

Si Flux vs Temp (b) 1993-l 994

0 5 10 15 20 Temp (“C)

n BH02 v BH03 * BH07-e BH08

Fig. 9. (a) Oxygen uptake versus bottom water temperature for all the stations and times, and (b) Si fluxes versus bottom water temperature.

iment redox potentials. Decreased sediment redox potentials favor surface-dwelling deposit feeders over deeper burrowing fauna (Pearson and Rosen- berg 1978). Decreased sediment redox potentials also result in an increase in sulfate reduction as a decomposition pathway leading to increased sulfur storage (discussed in Sampou and Oviatt 1991). Lower sediment redox and higher sulfides should in turn enhance the release of P through the dis- solution of iron minerals which adsorb P (Krom and Berner 1980). A higher percentage of the min- eralized DIN is released because of a decrease in the efficiency of denitrification at higher loading, although absolute rates of denitrification increase (Seitzinger and Nixon 1985). Because the majority of organic matter stored in sediments is not labile, a decrease in loading should lead to a fairly rapid decrease in sediment respiration (Kelly and Nixon 1984). In Kaneohe Bay, sediment respiration and nutrient fluxes showed marked decreases within 1 yr of sewage diversion (Smith et al. 1981). While

the three stations we examined over seasonal cycles exhibited some aspects expected from this general model, they also showed some important devia- tions from the expected patterns between fluxes and loading and Eh.

Station BH08 consistently had the lowest sedi- ment respiration rates and the least reducing con- ditions. Samples taken in August of each year (1992-1994) show no significant difference in res- piration rates between years. Animal abundances measured in August 1992-1994 were similar (Kropp and Diaz 1995). This station is furthest from the sludge disposal area, and organic matter deposition at this station may not have been af- fected by the cessation of sludge dumping in the harbor. DIC:DIN ratios at station BH08 during 1992 suggest relatively high denitrification rates, in accordance with relatively high Eh conditions. However, we observed high rates of P release, sug- gesting that the sediments were not retaining P in spite of the relatively oxidized nature of the sedi- ment. Sorption sites for P may be limiting P reten- tion at this station.

Organic matter loading at station BH03, the for- mer sludge disposal site, decreased dramatically af ter sludge discharge ceased in December 1991. Ox- ygen uptake and DIC release at station BH03 ex- hibited large year to year differences from 1992 to 1994, but contrary to expectations, there was no uniform reduction in respiration rates over time. In contrast, rates increased dramatically more than a year after discharge ceased. Both seasonal pat- terns and overall rates of respiration appeared to correspond with qualitative observations of animal abundances. In August and November 1992, when respiration for the year was the highest, high abun- dances of tube-dwelling amphipods and other in- fauna were noted. Respiration rates in the summer of 1993 were much higher than in 1992; infauna were also observed in higher numbers in 1993. In October 1993, the amphipods had largely disap- peared, and oxygen uptake rates dropped to below rates measured in November 1992 in spite of warmer temperatures in October 1993. Benthic an- imal abundances in the spring and summer of 1994 were lower than in 1993 and respiration rates were also lower until October, when divers report- ed a large increase in densities. This coincided with another peak in oxygen uptake despite lower water temperatures.

Sediment redox potential showed an inverse re- lationship to sediment respiration at station BH03 as previously described (porewater constituents and Eh). Sediment RQ and nitrate fluxes showed the expected relationships to Eh. In 1993, when sediments were more oxidizing than in 1992 or 1994, the RQ was less than 1 and there was a large

Benthic Metabolism and Nutrient Cycling 361

efflux of nitrate from sediments. In 1993 nitrate made up the majority of the DIN flux for the year (Table 2). Despite the more oxidizing conditions in 1993, the proportion of mineralized P that was released from the sediments was higher in 1993, and DIC:DIN flux ratios indicated that the relative proportion of mineralized N that was denitrified was lower (although absolute denitrification rates were higher, Nowicki personal communication; Gi- blin et al. 1994). During 1994 the sediments be- came more reduced, although the respiration rates were lower. In spite of the more reduced condi- tions, P release relative to respiration was lower in 1994 than in 1993.

We do not know if a significant amount of sludge reached station BH02, or if loading at this station was altered once discharge ceased. We observed less annual variation in fluxes at station BH02 than at station BH03. At station BH02 higher animal abundances were not associated with higher sedi- ment respiration rates. In fact the highest respira- tion rate measured at this station was in May 1993 when the sediments were devoid of macrofauna and surface sediments were highly reduced. In 1993, sediments at station BH02 had much lower rates of sediment metabolism than station BH03 but exhibited more reduced conditions and higher DIC:DIN flux ratios. In accordance with the gen- eral model described earlier, sediments from BH02 released large amounts of phosphate under the highly reducing conditions and showed a net stor- age of sulfur. In 1994, sediments from BH02 fol- lowed the expected pattern. With higher sediment Eh, there was less relative P release and the DIC: DIN flux ratio was higher. However, contrary to expectations, sediment RQ increased.

Some insight into the role animals have in these sediments can be observed by comparing diffusive fluxes calculated from porewater gradients (Klump and Martens 1981) with measured fluxes. Mea- sured fluxes of silica in July 1993 were four times higher than predicted at station BH02 and more than 25 times higher at station BH03. In July 1994 there was a sixfold difference between the mea- sured and calculated fluxes at station BH02, and a fivefold difference at station BH03. The difference between calculated and observed fluxes gives an indication of the importance of bio-irrigation oc- curring in the sediments.

It appears that the irrigational effects of benthic animals exert a strong control over sediment redox characteristics and flux ratios at these sites. This conclusion is similar to Sampou and Oviatt (1991)) who suggested that macrofauna may exert a stron- ger control on carbon respiratory pathways in sed- iments than does carbon loading. At our stations, high numbers of benthic animals were associated

with a high rate of net nitrification, and lower rel- ative retention of N. Presumably, the nitrified N was rapidly flushed from the sediments preventing extensive denitrification. The effect that animals have on nitrification and flux ratios depends upon many factors, including macrofaunal community structure and sediment organic matter quality (All- er 1982; Banta 1992), so it is difficult to generalize from our results. A number of other investigators have observed enhanced nit&cation in the pres- ence of animals, but in some cases denitrification is enhanced (Rristensen et al. 1991) while in other cases it is not (Banta 1992). In addition to altering microbial processes, benthic animals can alter nu- trient fluxes and flux ratios by directly ingesting organic matter and excreting inorganic nutrients (Gardner et al. 1993). When a high percentage of the sediment organic matter mineralization is car- ried out by animals in ventilated burrows, sediment nutrient trapping mechanisms such as denitrifica- tion and P adsorption are by-passed. Direct mac- rofauna decomposition may explain the relatively low retention of N and P at station BH03 during 1993.

The Importance of Benthic Fluxes in Boston Harbor

To calculate the importance of organic matter decomposition in the sediments to the carbon bud- get of Boston Harbor, we used average annual DIC fluxes from stations BH03, BH02, and BHOS. We assigned these rates in proportion to the relative area1 extent of depositional (51%), reworked (29%), or erosional (20%) sediments in Boston Harbor. We excluded 1993 BH03 data because we felt the very high rates at the sludge disposal site during this year were probably not representative of the depositional areas in the harbor as a whole. Weighted average sediment respiration was 56 mmol C m-* d-l in Boston Harbor.

Levels of primary production have been esti- mated to be 325 g C me2 ym1 (74 mmol C m-* d-l) in Boston Harbor (Michelson 1991). Sewage efflu- ent and other sources provide an additional 200 g C m-* yr-l (46 mmol C m-2 d-i) to Boston Harbor (Menzie et al. 1991, revised using Massachusetts Water Resources Authority Discharge Monitoring Reports for 1992). Comparison of loading to sed- iment respiration indicates that about 46% of the total organic matter entering the harbor from sew- age and primary production is mineralized on the bottom. This percentage is nearly twice as high as that reported from other estuaries (Nixon and Pil- son 1984). The reasons for such a high percentage of the decomposition to occur on the bottom is presently unexplained. It is possible that our sam- pling may have been biased toward more metabol-

362 A. E. Giblin et al.

ically active sites, but measurements at other sites (T4, R4, and T7) suggest that the primary sites, with the exception of BH03 in 1993, are represen- tative of the region. It is possible that the sedi- ments are currently out of equilibrium with inputs and that organic matter stored during decades of dumping is now being decomposed. Alternatively, the recent increases in animal abundances throughout the harbor may have enhanced the capture of organic matter to sediments through fil- ter feeding.

In spite of the role of the benthos in carbon cycling, it is less of a factor in N and P cycling in Boston Harbor. Although remineralized nitrogen from the sediments could supply a major portion of the phytoplankton demand for N (40%) and P (29%)) the absolute contribution of N and P from the benthos is small compared to the allochthonus inputs. At the present time new nitrogen and phos- phorus inputs to the harbor (Alber and Chan 1994) are an order of magnitude greater than the benthic flux of N and P and external inputs exceed phytoplankton N and P requirements.

The regeneration of Si from sediments can sup- ply a significantly greater fraction of the Si re- quired to support primary production than N or P regeneration supports primary production. On average, benthic silica fluxes could supply more than 60% of the Si requirements for primary pro- duction, assuming that the production was com- pletely dominated by diatoms. Currently, silica in- puts to the harbor from wastewater discharge are considerably lower than N inputs: an average N:Si ratio of 3.44 (Hunt et al. 1995). In contrast, annual average N:Si release ratios from the sediments ranged from 0.53 to 1.15. However, benthic fluxes are four times lower than Si inputs from wastewa- ter.

The high rates of anthropogenic nutrient inputs to Boston Harbor greatly exceed the capacity of the sediment to remove nutrients through denitri- fication and/or burial. The average area-weighted value we calculate for N removal from the harbor using DIC:DIN ratios is 4.0 mmol mm2 d-l, sug- gesting that denitrification accounts for about 1’7% of the nitrogen load of the harbor. Although this estimate of N removal in the harbor is somewhat higher than direct N, flux measurements (Nowicki 1994; Giblin et al. 1995)) it supports the conclusion that the majority of the nitrogen entering Boston Harbor is exported to Massachusetts Bay (Kelly 199’7). The area1 average of the P fluxes from the three primary stations indicated there was no net removal of P from the harbor during 1992-1994. Sediments served as a net source of P, releasing an average of 0.22 mmol m-2 d-l.

ACKNOWLEDGMENTS

We would like to thank David Giehtbrock for field assistance, and for carrying out many of the chemical analyses. David Olm- stead provided expert help as master of the R/V Asterias. Ann Spelecy, Jack Bectold, and Scott Libby provided help in the field and with the BOSS navigation system. We thank Jack Kelly and Barbara Nowicki for sharing unpublished data with us and for their insights and useful discussions on the data. We thank Mi- chael Mickelson for his careful comments on earlier technical reports, and two anonymous reviewers for constructive com- ments. Financial support was provided by the Massachusetts Wa- ter Resources Authority and NOAA Sea Grant.

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Received for consideration, January 29, 1996 Accepted for publication, October 25, 1996