Community oxygen metabolism in a shallow tidal estuary

Estuarine, Coastal and Shelf Science (1988) 27.33-43

Community Oxygen Metabolism Shallow Tidal Estuary

B. E. Kenney,

W. Litaker”

C. S. Dukeb

Botany Department and Marine Laboratory, 28516,U.S.A. Received 24January

in a

and J. Ramus

Duke University, Beaufort, NC

1987 and in revisedform 19January

1988

Keywords: oxygen balance; metabolism; annual variations; tion; tidal estuaries; lagoons; North Carolina Coast

plankton

produc-

Comprehensive sampling of a shallow tidal estuary was performed hourly for 14 days, at three-month intervals throughout the annual temperature cycle. The project took place in the Newport River estuary located inside the Outer Banks of North Carolina, U.S.A. In all 26 parameters were monitored at a single station, including meteorology, hydrology, water chemistry and phytoplankton production physiology. The estuarine character in colder months was dominated by riverine input, while in warmer months the estuary was lagoonal, having limited input and exchange with the sea. A holistic evaluation of estuarine community 0, metabolism was developed using diffusion-corrected changes in 0, concentration. These data indicated positive integrated die1 production (autotrophy) only in winter (February). The estuary was functionally heterotrophic during warmer months (May, August, November). Integrated short-term radiocarbon productivity estimates compared favorably with measurements of oxygen based die1 gross production rates. Community 0, based respiration rates (heterotrophy) exhibited a strong positive relationship with water temperature. During summer, rates of heterotrophic metabolism and associated nutrient regeneration appeared to control autotrophic production.

Introduction Estuaries simultaneously receive terrestrial runoff waters and exchange waters with the continental shelf and surrounding marshes. The ultimate sources of plant nutrients and inorganic carbon are allochthonous; however, autochthonous processes do regenerate nutrients for in situ consumption. Estuarine community 0, metabolism, a composite of gross productivity and respiration, is subject to many forces in time and space, and the scale of variability can be particularly fine for shallow tidal estuaries. Strong tidal currents, large runoff volumes and wind-driven advection rapidly mix waters and can destroy vertical temperature and salinity gradients. Benthic processes can be tightly coupled with ‘Present address: Department of Microbiology & Immunology, School of Medicine, 609 Faculty Laboratory Office Building 231 H, University of North Carolina at Chapel Hill, Chapel Hill, NC 27514, U.S.A. *Present address: Department of Biological Sciences, Wellesley College, Wellesley, Mass 02181, U.S.A. 33 0272-7714/88/070033+

11 $03.00/O

@ 1988 Academic Press Limited

34

B. E. Kenney et al.

water column processes, and the water column interacts with the atmosphere. The hierarchy of control variables or forcing functions is dominated by the annual temperature cycle, which determines the character of the estuary (Boynton et al., 1982) at any moment in time. Thus short- and long-term sampling are required to resolve the many scales of variability. A coherent view of estuarine dynamics is revealed only when the time constants of sampling match those of physical, chemical and biological processes (Harris, 1980). A case in point is the Newport River estuary, located in the Outer Banks region of North Carolina. A comprehensive time-intensive sampling program was conducted to resolve the role of hourly and seasonal variability in phytoplankton ecology (Litaker et al., 1987). The Newport River estuary is dominated by riverine inputs in winter, and phytoplankton growth-limiting nitrogen (N) is supplied as nitrate (NO;) and ammonium (NH,+) by runoff from the watershed. In summer, the estuary is lagoonal, with limited river input and exchange with the sea, and N is supplied as NH,+ by biological regeneration. Chlorophyll-u (chl-a) biomass varied over the 4-10 day period in winter, corresponding to passage of atmospheric fronts, associated precipitation and runoff. In summer, chl-a biomass varies at the die1 period, corresponding to the day/night cycle. Although finely tuned to environmental variability, phytoplankton abundances were at equilibrium in that daily chlorophyll production was balanced by daily loss due to grazing, export and deposition. Given that an estuary is the sum of many component processes, variable at several temporal and spatial scales, and that the system undergoes fundamental changes during the annual cycle, can the fundamental character of such a system be treated holistically? An holistic evaluation of estuarine metabolism relies on the measurement of integrative processes, such as total-system 0, and CO, exchange. If a body of water is sufficiently shallow or fertile, then metabolic activity should be readily detectable as changes in the mass-balance of the water column values of dissolved 0, or CO,. Determination of community 0, metabolism rates based on variation in dissolved gases have been termed the ‘free water’ method of assessment (Hall & Moll, 1975). Free-water methods using combinations of dissolved 0, (DO) and pH changes have been used to assess community 0, metabolism in diverse environments, including coastal lagoons (Odum & Hoskins, 1958), estuaries (Kemp & Boynton, 1980) and mesocosms simulating estuaries (Oviatt et al., 1986). In this work we investigated the effect of physical, chemical and biological processes, at various time scales, on total-system 0, metabolism of the Newport River estuary, NC.

Materials

and methods

High-frequency sampling was performed in a shallow tide-flushed estuary in the Outer Banks region of North Carolina, U.S.A. (Litaker et al., 1987). Because of its exposure and geomorphology, the Newport River estuary probably represents an extreme of the category ‘river dominated’ estuary (Boynton et al., 1982). This estuary has a surface area of 30 km2, an average MLW depth of 1 m and is surrounded by Spurtinu ulternzj7oru marsh. The estuary drains a watershed of 300 km2, composed of lowland longleaf pine forest (Croatan National forest), farmland and pocosin. Water draining into the estuary is highly colored by humic substances; continental shelf water is supplied daily through Beaufort Inlet. Estuarine circulation is dominated by two lunar tides per day which have an average

Estuarine community metabolism

35

amplitude of 0.8 m. Current velocities average 0.3-0.4 m s-l, and range from 0 to 1 m ss’, sufficiently energetic to destroy vertical temperature and salinity gradients (Wolfe, 1975). Five 14-day sampling cruises were conducted, cued to the annual cycle in water temperature, in February, May, August and November 1982, and February 1983. Twentysix parameters were monitored on an hourly basis (24 samples per day) including meteorology, hydrology, water chemistry and phytoplankton physiology. A floating laboratory remained on a mid-estuary station (34”46’N, 76”42’W) for the duration of each cruise. Mid-depth water samples were taken with a horizontal van Dorn bottle, and temperature and DO were determined immediately with a polarographic sensor (YSI 5750) and meter (YSI 57). An Orion temperature-compensated meter was used for pH. Salinity was determined by conductivity (Beckman Industrial Instruments RS-5-2 induction salinometer). Turbidity was measured as NTU with a HF Instruments DRT-100 nephelometer. Current velocity was obtained from a calibrated biplane current cross, and wind velocity from a calibrated anemometer on site. Chl-a was determined by fluorometric analysis (Turner Designs 111 fluorometer) of particulate material collected on Gelman A-E glass fiber filters by gentle suction and extracted into 90% acetone. The flushing time, i.e. the time required to replace the existing estuarine freshwater, was calculated by the riverine discharge method of Aston (1978), and using the runoff estimates given in Litaker (1986). Radiocarbon productivity On alternate days, radiocarbon fixation measurements were made, beginning at dawn. Every three hours throughout the day, six 125-ml Wheaton bottles with Teflon-lined caps were filled from the sample bottle. The bottles were inoculated with 5 uCi H’%O; and placed in a neutral density screen series (0,5,15,30,50, and 100% of ambient light) in an unobstructed clear Plexiglas incubator. Incubation temperature was controlled by continuously pumping ambient estuarine water through the chamber. After a 2.5-h incubation, 25-ml samples from each bottle were filtered through 25-mm Gelman A/E filters, washed with 10 ml isotonic seawater containing excess MgCO,, and placed in 10 ml of Aquasol-2. Specific activities were determined from l-ml subsamples taken immediately after inoculation and neutralized (0.5 ml of O-1 N NaOH) to prevent loss of activity. Quench corrections were done by determining the efficiency vs. H number regression of a 14C-toluene quench series. Radioactivity was counted on a Beckman LS 8000 liquid scintillation spectrometer. Die1 depth-integrated productivity was calculated using mean values of Secchi depths, incident light and depth determinations recorded during each incubation. The total daily productivity was determined by trapezoidal integration over short-term incubations. The average water column light levels were determined according to Riley (1957). Community oxygen metabolism In all cases of free-water metabolism analysis, raw estimates of changes in dissolved 0, must be corrected for net gas exchange (diffusion) across the air-water interface (Hall & Moll, 1975). The impact of water movement on net gas diffusion is of primary importance, i.e. horizontal water movement can account for roughly half the net 0, flux (Kemp & Boynton, 1980). DiToro et al. (1977) have provided the following equation for the diffusion coefficient, an accepted predictor of potential net gas exchange across an estuarine air-water interface (Bowie et al., 1985):

36

B. E. Kenney

et al.

Kc,,, = (DL Y/Hy5

(1)

where DL is molecular diffusivity [2.1 x lop5 cm’ s- ’ for 0, in seawater at 20°C based on Broecker & Peng (1982)]. I’ is current speed and H is water depth. This coefficient is corrected for temperature deviation (DiToro et al., 1977): K = K

1.024tT-201

(20)

(2)

where T is temperature (“C). The diffusion coefficient (h -‘) multiplied by the apparent O3 utilization (AOU) value, i.e. (C,,,- C) in mg lo- *, generates a net diffusion rate which is used to correct the gross rate of O2 concentration change (mg 0, l- ’ h ‘). Oxygen saturation values (mg 1~ i) were calculated as a function of temperature and salinity from the empirical algorithm provided by Kester (1975). Instantaneous rates of 0, change were calculated for each hourly sample with a fiveelement cubic differencing filter (Savitsky & Golay, 1964) following outlier removal by wild-point editing and application of a nine-element cubic smooth, thus removing most high-frequency noise without damping the signal (Figure 2). This method uses adjacent intervals to determine a slope or rate at each sample point under consideration, and is less subject to random fluctuation than is slope determination via simple forward difference techniques (Shukla & Rusling, 1984). Single-curve analysis of stream metabolism (Odum, 1956) assumes stream homogeneity. Similarly, based on mid-depth trawl transect studies (Hyle, 1976), the bulk of the Newport River estuary experiences a simultaneous change in dissolved Oz. Thus, community metabolism was calculated as a single-station DO change, according to minor modification of methods established by Odum (1956) and Beyers (1963). The first phase was the determination of the apparent 0, utilization (AOU) value, which was calculated as sample DO (mg 1~ ‘) minus DO at saturation. The second phase involved calculation of the diffusion coefficient (K) according to the equation: K(h-- I) = (0.0272

v/H3)‘) 5 1.024(~‘-~~’

(3)

where I/ is current velocity (m s ‘), His water height (m), and T is temperature ( C). The product of K and AOU is the diffusion rate which is used, in turn, to correct the raw 0, exchange rate to yield an instanteous gas-exchange rate attributable to community Oz metabolism (mg 0, 1-l h ‘) at each hourly sample interval. There is a proliferation of coefficients that have been used under differing conditions of flow rate, water depth, wind stress and temperature (Bowie et al., 1985). Most such coefficients are empirical relationships using current speed and water depth. Some correction algorithms are independent of physical parameters, but make specific assumptions about the photosynthesisirradiance relationship that may be equally objectionable (Kosinski, 1984).

Results The water temperature oscillated on an annual cycle between mean February lows of 10.8”C and mean August highs of 27.2”C, with values rising in May and declining in November (Figure 1). Likewise, salinities oscillated between mean values of 15 and 34 ppt, with an annual pattern similar to temperature. The standing phytoplankton biomass was generally highest in February and lowest in November, with intermediate values in May and August (Figure 1). DO and 0, saturation showed an inverse pattern to

37

Estuarine community metabolism

(e) I +y i Feb May 1982

Aug NW

Feb 1983

%b May

Aug Nov

1982

Figure 1. Means and standard errors of selected (a) Water temperature; (b) chl-a; (c) salinity; metabolism (COMET); (f) oxygen saturation.

Feb

60

1983

features in the Newport River (d) turbidity; (e) community

estuary. oxygen

temperature and salinity, being highest in February, lowest in August and intermediate in November and May (Figure 1). The diffusion-corrected 0, concentration change or community 0, metabolism rates, calculated from smoothed time-course data (Figure 2), provided integrated estimates of die1grosscarbon fixation (PQ assumedto be 1.25) that are comparable (r = 0.94, p = 0.0 17) to simultaneous integrated die1 14Cproductivity estimatesasshown in Table 1. Volume-specific community 0, metabolism (mg 0, 1-l h-i) always showed a distinct die1 (24-h) cycle, being lowest around sunrise and highest after solar noon. In general, estuarine community metabolism shifted from heterotrophy during the night to autotrophy during the day (Figure 3). In winter sampling periods, the estuary was a net producer of 0,, i.e. it wasfunctionally autotrophic (Figure 3). Die1 integrated metabolism averaged 0.37 and 0.99 mg 0,1-t day-’ in February 1982 and 1983, respectively (Table 1). However, for the greater part of the year, the estuary was a net consumer of O,, i.e. it was functionally heterotrophic (Figure 3, Table 1). Die1 integrated metabolism averaged -0,53, - 0.77 and - 0.53 mg 0, 1-l day-’ in May, August and November, respectively. This was a result of a dramatic seasonalincrease in the estimated community respiration that transcended a more modest seasonalincrease in the estimated grossphotosynthetic performance (Table 1). Daily estuarine temperature data for 12 months during the study was plotted as a frequency histogram [Figure 4(a)], indicating a bimodal distribution with a yearly median daily mid-range temperature of 18.8”C. Gross production and community respiration

38

et al.

B. E. Kenney

I I

13

15

17

19

21

23

25

IO May

-i

1982

8 L.. 6 11 ’

.’ /

41

I

15

E”

IO

ti z

*-

zo

6-

-

_> ::4Efn

:.

. .

.

1

17

August

IO

.

I

I

I

19

I

21

. /

I

23

,

/ 25

,

,

27

29

1982

”

I2

’

”

”

11

11

/

I

14

16

I8

20

22

9

II

13

15

I7

I 24

12 I---- November

1982

IO

5

7

14 7 - February 12 - .

8”

30

1982

”

Figure 2. Dissolved nations. Calculated

TABLE periods

1. Community

”

3

”

”

5

’

7

9

’

’

II

”

I3

oxygen data plotted with the smoothed line used for rate determisaturation values are represented by the nearly linear plot.

oxygen

metabolism

February 1982 Integrated die1 rateY Community gross photosynthesis” Community respiration” Autotrophy ratio (Pg/Rs) Oxygen based gross photosynthesis Radiocarbon gross photosynthesis

19

(as gC m ’ d ‘)” (as gC m ’ d ‘)”

0.3742 16747 1.3005 1.29 O-81 0.59

values

integrated

over

May 1982

August 1982

-0.5310 2.3733 2.9004 0.82 1.17 1.80

PO.7676 2.9562 3.7238 0.79 1-54 1.86

“Values in mg 0,l ’ day ‘. “Conversion of O? derived gross photosynthesis radiocarbon uptake rates assumes PQ = 1.25.

rates

for

two-week

November 1982 ~-0.5308 0.8705 1.4013 0.62 0.45 0.34

comparison

sampling

February 1982 0.9861 1.3565 0.3704 366 0.61 0.64

with

the

Estuarine community metabolism

39

0 -0.1

^ I,

-0.2

5

November

1982

0

0

06.00

12.00 Time

18.00

24.00

of day

Figure 3. Means and standard errors of hourly five cruises. Stippled areas indicate community community respiration.

community oxygen metabolism for the gross production. Striped areas indicate

rates plotted as a function of temperature [Figure 4(b)] suggestthat the Newport River estuary experienced a shift in community 0, metabolism from autotrophy toward heterotrophy for most of the year. Discussion and conclusions Two physical factors dominated whole-system 0, metabolism in the Newport River estuary, viz. the daily course of insolation and the annual temperature cycle. The primary source of daily variation of DO within the water column was photoautotrophy. Community respiration is assumedto be a relatively constant consumer of water-column DO at the die1scale.Thus the estuary had background net heterotrophy offset by daytime cycles of net photoautotrophy, and community 0, metabolism rates declined at night and increased during the day. Heterotrophy within the water column was positively temperature dependent; thus DO consumption rates were highest in August, lowest in February, and intermediate in May and November. The estimated gross photosynthesis rates followed an annual

40

B. E. Kenney et al.

0.08

t

g

0.06

z

0.04 0.02

4 t~~ill~~~~~~~~~~~~~~lill~~~~~~l~t 0

IO Water

20 temperature

30 (“C)

Figure 4. (a) Daily mid-range temperature plotted as a yearly frequency histogram. The median value (18.8 ,‘C) is indicated by the arrow. (b) Oxygen derived gross photosynthesis (i 1) and respiration ( W) plotted as a function of temperature.

pattern, being highest in August and May, and lowest in November and intermediate in February. Thus, the die1 integral of community 0, metabolism, the net DO debt or surplus, varies with season. The mean die1 integral of community 0, metabolism was nearly inversely proportional to temperature (Figure 1). Estuarine community 0, metabolism at the die1 scale was net heterotrophic during May, August or November, and made up the debt by taking in atmospheric 02. In February, the community 0, metabolism was photoautotrophic, on balance, with a net loss of 0, to the atmosphere. In February the estuary was riverine, i.e. runoff from the watershed caused a net flux of water seaward. The flushing time for freshwater exchange in February 1982 was estimated at 8.4 days, assuming a 70”,, runoff volume given in Litaker (1986). At this time of year, productivity was regulated by NH: and NO, carried into the estuary by runoff waters. Carbon fixed in situ was exported from the estuary or deposited to sediments, in situ heterotrophy was low, thus there was a net flux of 0, to the atmosphere. In August, the estuary was lagoonal, X~SU Boynton et al. (1982), i.e. there was little net flux of water seaward and little DIN loading from the watershed. The flushing time for freshwater exchange in August 1982 was greater than 480 days. Nitrogen was supplied to the water column by remineralization of in situ productivity, primarily as NH: (Litaker et ul., 1987), a strongly heterotrophic process (Nixon, 1981). At this time of year, carbon fixed in situ was consumed in situ, and 0, was imported from the atmosphere. Thus, two primary factors contribute to the strong heterotrophic nature of the estuary during summer, respiration of previously fixed organic carbon and in situ consumption of productivity. Seasonal alteration between late winter, when autotrophic (riverine) conditions dominate, and summer, when heterotrophic (lagoonal) processes prevail, is consistent with the correlation analysis of Boynton et al. (1982). These authors correlated plankton productivity and biomass with several physical and nutrient variables from 63 estuarine

Estuarine community metabolism

TABLE

variables (SECCHI rates

41

2. Partial correlation analysis of community oxygen metabolism zrs. selected shows the importance of incident irradiance (PAR), light attenuation and TURBIDITY) and wind speed on hourly community 0, metabolism

Tide Temperature Salinity Current Wind PAR SECCHI TURBIDITY Chl-a PHAEO NH, NO,+NO, PO* SIO, Significant “Significant

February 1982

May 1982

- 0.099 0.013 - 0.020 0.018 0.262b 0.445b 0.437b -0.189b -0.131” - 0.084 0.037 -0.113 -0.068 0.146”

0.045 0.127 - 0.046 - 0.075 0.5866 0.767’ 0.577” 0.209” 0.365b -0.241b - 0.245b 0.025 -0.1776 0.086

at the at the

August 1982

November 1982

February 1982

0.143” 0.017 0.09 1 0.068 0,421b 0.835’ 0.669b 0.076 0.344” - 0.4306 -0.19@ - 0.062 - 0.2016 - 0.062

0.164b 0.081 0.103 - 0,093 0.348’ 0.5996 0.58Sb 0.207’ 0.023 - 0.002 -0.178b -0.1526 -0.125” - 0.093

-0.211b -0,018 - 0.082 0.012 -0.022 0.489’ 0.278b -0.123” -0,102 -0.21Y -0.120” -0.130” -0.025 0,192b

p = 0.05 level. p = 0.01 level.

systems.The analysis showed that river-dominated estuarieshave a strong positive correlation between seasonal primary production rates and water-column nitrate, light attenuation and directional river flow rate. On the other hand, lagoonal estuaries show strong negative correlations between seasonalproduction and water temperature, DIN and incident irradiance. Our analyses (Table 2) indicate that incident irradiance and attenuation are important correlates with community metabolism, along with wind speed and nutrient availability. As with all estuaries reviewed by Boynton et al. (1982), high net carbon production occurred simultaneously with maximum chl-a in the Newport River (Litaker et al., 1987). However, we report here a clear reversal of the positive correlation of seasonaltemperature vs. chl-a and net carbon production reported for the Newport River and other estuaries (Thayer, 1971). With an appropriate sampling regime, yearly maxima of chl-a biomassand net production appear in colder months. One reason for this apparent disparity is the dominance of an increased respiration signal seen by community 0, metabolism analysis during the warmer periods (May, August). Community 0, metabolism values are, insofar asalgorithms allow, corrected for effects of physical factors on net 0, exchange acrossthe air-water interface. The impact of 0, producing and consuming processesslightly lagged (l-3 h) the light-dark cycle. The die1 cycle of community metabolism rates declined to a net 0, consumption at night during all periods

except

February

1983

(Figure

3) when

it remained

near

zero

at night.

It was only

during this sampling period that the air temperature was significantly below mid-depth water temperature, cooling the surface waters which then served asa barrier to outgassing of 0, and which raised the apparent baselineof community 0, metabolism. Experimental ecosystems simulating Narragansett Bay have shown an annual 0, metabolism cycle that includes periods of net community heterotrophy (Oviatt et al., 1986). The control (unenriched) MERL mesocosmswere net autotrophic in winter months (January-April), corresponding to the lowest annual water temperatures, as has

42

B. E. Kenney

et al

been shown in this study. During the rest of the year, the systems were net heterotrophic, and maximal in July-September when water temperatures were at their annual high. Enrichment with NH,+, PO; and SiOi(N:P:Si atom ratios 13:l:l) to eight-fold influent concentrations progressively increased the amplitudes of the annual autotrophyheterotrophy cycle and benthic respiration was proportionately more active. Nutrient enrichment increased 0, production rates within the mesocosms, but water-column 0, consumption by bacteria also increased proportionately. Although both 14C production and carbon fixation values derived from community 0, metabolism showed increased gross production during warmer months (Table 1); community respiration was likewise greatly increased, and carbon fixation rates were not high enough to support heterotrophic consumption. The estuary was a net carbon sink, possibly through bacterial decomposition of POC and DOC imported from surrounding Spartina alterni’ora marshes (Turner, 1978). Our data indicate that radiocarbon assessment of primary production by phytoplankton ignores a major source of the organic carbon supply to higher trophic levels. Thus, community metabolism studies have an advantage over r4C methods in assessing availability of fixed carbon, as such studies evaluate the input of many ecological factors (Williams et al., 1979). Phytoplankton productivity in the Newport River estuary is nitrogen limited. When the estuary is lagoonal in summer, phytoplankton productivity is at an annual high. The N:P atom ratios for residual water-column nutrients are very low, cycling from a mean value of 4 at dawn to a mean value of 1 by mid-day (Litaker et al., 1987). Photoautotrophic assimilation draws residual nitrogen levels down to near-detection limits during the day, while heterotrophic regeneration continually replenishes the stock. It follows that the rate at which growth-limiting nutrients (such as nitrogen) are assimilated by photoautotrophs exceeds the rates by which nutrients are liberated by heterotrophs. Thus, it is the rate of heterotrophy which limits the rate of autotrophy, and it is temperature which limits the rate of heterotrophy within the estuary. Kemp and Boynton (1980) point out specific problems of horizontal dispersion as a result of high flow rates that may interfere with free-water community metabolism techniques, but find that this must be weighed against the general underestimation of metabolic rates of production and respiration that can result from discrete bottle determinations. However, free-water estimates provide a means for conducting whole-system analyses, in this case generating a view of the Newport River estuary as a nitrogen limited net carbon sink at the annual level, with high, temperature-cued rates of both gross photosynthesis and community respiration at the die1 scale.

Acknowledgements We thank Dr W. Kirby-Smith for unpublished daily temperature and salinity data, and R. T. Barber and W. M. Kemp for their critical review of the manuscript. Support from NSF grant OCE-81-13328 to JR is acknowledged.

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Estuarine

community

metabolism

43

Bowie, G. L., Mills, W. B., Porcella, D. B., Campbell, C. L., Pagendorf, J. R., Rupp, G. L., Johnson, K. M., Chan, P. W. H., Gherini, S. A. & Chamberlin, C.E. 1985 Rates, Constants and Kinetics Formulations in Surface Water Quality Modeling, 2nd edn. United States Environmental Protection Agency, EPA/660/3-85/040. Boynton, W. R., Kemp, W. M. & Keefe, C. W. 1982 A comparative analysis of nitrienrs and other factors influencing estuarine phytoplankton production. In Estuarine Comparisons (Kennedy, V. S., ed.). Academic Press, New York, pp. 229-250. Broecker, W. S. & Peng, T.-H. 1982 Tracers in the Sea. Eldigio Press, Columbia University, New York. DiToro, D. M., Thomann, R. V., O’Conner, D. J. & Mancini, J. L. 1977 Estuarine phytoplankton biomass models-verification analysis and preliminary applications. In The Sea: Ideas and Observations on Progress in the Study of the Seas. Vohone 6. Marine ModelZing (Goldberg, E. D., McCave, I. N., O’Brien, J. J. & Steele, J. H., eds). Wiley, New York, pp. 969-1020. Hall, C. A. S. & Moll, R. 1975 Methods of assessing aquatic primary productivity. In Primary Productivity of the Biosphere (Lie& H. & Whittaker, R. H., eds). Springer-Verlag, New York, pp. 19-53. Harris, G. P. 1980 Temporal and spatial scales in phytoplankton ecology. Mechanisms, methods, models and management. CanadianJournal of Fisheries and Aquatic Science, 37,877-900. Hyle III, R. A. 1976 Fishes of the Newport River estuary, North Carolina. Their composition, seasonality and community structure, 1970-1972. Ph.D. thesis, University of North Carolina, Chapel Hill, NC. Kemp, W. M. & Boynton, W. R. 1980 Influence of biological and physical processes on dissolved oxygen dynamics in an estuarine system: Implications for measurement of community metabolism. Estuarine and Coastal Marine Science 11,407-431. Kester, D. A. 1975 Dissolved gases other than carbon dioxide. In Chemical Oceanography, Volume 2,2nd edn. (Riley, J. I’. & Skirrow, G., eds). Academic Press, New York, pp. 497-556. Kosinski, R. J. 1984 A comparison of the accuracy and precision of several open-water oxygen productivity techniques. Hydrobiologia 119,139-148. Litaker, R. W. 1986 Dynamics of a well-mixed estuary. Ph.D. thesis, Duke University, Durham, NC. Litaker, W., Duke, C. S., Kenney, B. E. & Ramus, J. 1987 Short-term environmental variability and phytoplankton abundance in a shallow tidal estuary. I. Winter and summer. Marine Biology 96,115-121. Nixon, S. W. 1981 Remineralization and nutrient cycling in coastal marine ecosystems. In Estuaries and Nutrients (Nielson, B. J. & Cronin, L. E., eds). Humana Press, Clifton, NJ, pp. 111-138. Odum, H. T. 1956 Primary production in flowing water. Limnotogy and Oceanography 1,102-l 17. Odum, H. T. & Hoskins, C. M. 1958 Comparative studies on the metabolism of marine waters. institute of Marine Science Publications. (University of Texas) $16-46. Oviatt, C. A., Rudnick, D., Keller, A., Sampou, P. & Almquist, G. 1986 A comparison of system (0, and CO,) and C-14 measurements of metabolism in estuarine mesocosms. Marine Ecology-Progress Series 28, 57-67. Riley, G. A. 1957 Phytoplankton of the north central Sargasso Sea. Limnology and Oceanography 2,252-270. Savitsky, A. & Golay, M. J. E. 1964 Smoothing and differentiation of data by simplified least squares procedures. Analytical Chemistry 36,1627-1639. Shukla, S. S. & Rushng, J. 1984 Analysing chemical data with computers: Errors and pitfalls. Anafyticat Chemistry 56,1347A-1368A. Thayer, G. W. 1971 Phytoplankton production and the distribution of nutrients in a shallow unstratified estuarine system near Beaufort, N.C. Chesapeake Science 12,240-253. Turner, R. E. 1978 Community plankton respiration in a salt marsh estuary and the importance ofmacrophytic leachates. Limnology and Oceanography 23,442-451. Williams, P. J. leB., Raine, R. C. T. & Bryan, J. R. 1979 Agreement between the “C and oxygen methods of measuring phytoplankton production: reassessment of the photosynthetic quotient. Oceanologica Acta 2, 41 l-416. Wolfe, D. A. 1975 Modelling the distribution and cycling of metallic elements in estuarine ecosystems. In Estuarine Research, Volume 1 (Cronin, L. E., ed.). Academic Press, New York, pp. 645-671.