MARINE ECOLOGY PROGRESS SERIES Published June 26 Mar Ecol Prog Ser

Carbon cycling in a tidal freshwater ecosvstem: a carbon cras flux studv

Scott C. Neubauerl,*,W. David ille er^^**, Iris Cofrnan Anderson'

'Virginia Institute of Marine Science, SchooI of Marine Science, College of William and Mary, Gloucester Point, Virginia 23062, USA '~e~artrnentof Biology, College of William and Mary, Williamsburg, Virginia 23187, USA

ABSTRACT: A process-based carbon gas flux model was developed to calcuIate total macrophyte and microalgal production, and community and belowground respiration, for a Peltandra virginica domi- nated tidaI freshwater marsh in Virginia. The model was based on measured field fluxes of CO2 and CH,, scaled to monthly and annual rates using empirically derived photosynthesis versus irradiance, and respiration versus temperature relationships. Because the gas exchange technique measures whole system gas fluxes and therefore includes turnover and seasonal translocation, estimates of total macrophyte production will be more accurate than those calculated from harvests. One limi- tation of the gas flux method is that gaseous carbon fluxes out of the sediment may underestimate true belowground respiration if sediment-produced gases are transported through plant tissues to the atmosphere. Therefore we measured gross nitrogen mineralization (converted to carbon units using sediment C/N ratios and estimates of bacterial growth efficiency) as a proxy for belowground carbon respiration. We estimated a total net macrophyte production of 536 to 715 g C m-' yr-', with an addi- tional 59 g C m-' yr-' fixed by sediment microalgae. Belowground respiration calculated from nitrogen mineralization was estimated to range from 516 to 723 g C m-2 yr-' versus 75 g C m-' yr-l measured directly with sediment chambers. Methane flux (72 g C m-' yr-') accounted for 11 to 13% of total below- ground respiration. Gas flux results were combined with biomass harvest and literature data to create a conceptual mass balance model of macrophyte-influenced carbon cycling. Spring and autumn translocation and re-translocation are critical in controlling observed seasonal patterns of above and belowground biomass accumulation. Annually, a total of 270 to 477 g C m-2 of macrophyte tissue is available for deposition on the marsh surface as detritus or export from the marsh as particulate or dis- solved carbon.

KEY WORDS: Peltandra virginica . Macrophyte and microalgal . Carbon dioxide . Methane . Belowground respiration . Translocation . Sweet Hall marsh, Virginia

INTRODUCTION South Carolina and Georgia (Odum et al. 1984).In con- trast with east salt , which are dominated Tidal freshwater marshes are located at the head of by one (generally Spartina alternrflora) or several (i.e. the estuarine gradient where a suitable combination S. patens and Distichlis spicata) macrophyte species, of freshwater supply and tidal range permits their it is not unusual to find 50 to 60 plant species in a fresh- development. On the eastern of North water marsh (Pickett 1984, Perry 1991).Dominant veg- America, the most expansive tidal freshwater marshes etation changes seasonally and can include fleshy are located between New Jersey and Virginia and in broadleaf plants such as Peltandra virginica, Pontede- cordata, and Sagittaria latifolia and grass-like spe- cies such as Leersia oryzoides, Phragmites australis, 'E-mail: [email protected] "Present address: University of Maryland Center for Envi- latifolia, and Zizania aquatica. ronmental Science, Horn Point Laboratory, Cambridge, Intertidal salt and freshwater marshes have long Maryland 21613, USA been considered highly productive ecosystems. Salt

O Inter-Research 2000 Resale of full article not permitted 14 Mar Ecol Prog Ser

marshes dominated by monospecific stands of Spartina As an alternative to harvest methods, fluxes of CO2 alterniflora have been well studied, with aboveground and CH, have been used to estimate gross and net plus belowground net macrophyte production ranging macrophyte productivity under ambient field condi- from 1000 to 8000 g dw m-2 yr-' (Schubauer & Hopkin- tions (Blum et al. 1978, Giurgevich & Dunn 1978, son 1984).Most measurements have been made using Howes et al. 1984, Whiting & Chanton 1996) or under a variety of biomass harvest techniques which have experimental conditions such as elevated atmospheric been shown to produce estimates of plant productivity CO2 concentrations (Drake 1984, Curtis et al. 1989, that can exceed the physiological capacity of S. alterni- Azc6n-Bieto et al. 1994) or manipulated soil salinities flora (Morris et al. 1984, Dai & Wiegert 1996). Fewer (Pezeshki 1991, Hwang & Morris 1994). The carbon data are available for tidal freshwater marshes, due in gas flux technique integrates processes that occur part to their high diversity, seasonally variable species within and between aboveground and belowground composition, and patchy distribution of belowground compartments (e.g. turnover and translocation) and biomass. Reported annual net aboveground produc- therefore provides a more reliable estimate of total tion varies by species, averaging 900 g dw m-2 yr-' for production than harvest methods. If carbon fluxes from Peltandra virginica to 1900 g dw m-2 yr-' for Phrag- the sediments are measured in situ, sediment rnicro- mites australis (Whigham et al. 1978). Although few algal production can also be calculated (Anderson et studies have included belowground production, Booth al. 1997). (1989) reported approximately equal rates of above- Marsh macrophyte and microalgal organic matter ground and belowground production (1634 and 1568 g (carbon) can undergo several potential fates: biotic dw me2 yr-', respectively) for a monospecific stand of remineralization to CO2 and CH,, retention in the P. virginica in Virginia. When belowground components marsh system (as accumulated biomass or sediments), are included, it appears that freshwater marshes are as consumption by herbivores, or export to adjacent river- productive as salt marshes. ine and estuarine environments as particulate (POM) Determining community production in tidal fresh- or dissolved organic matter (DOM). The outwelling water marshes is, at best, a difficult proposition due to hypothesis, which proposes that marsh-derived ma- the diverse and seasonally changing species composi- terials can support secondary production in nearby tion and the extensive yet patchy distribution of below- aquatic communities, requires a net export of organic ground biomass (de la Cruz 1978,Whigharn et al. 1978). materials from the marsh (e.g.Teal 1962, Odum 1968, Most commonly, aboveground production has been Gosselink et al. 1973).Although historically developed measured using either single or multiple harvests for estuarine and systems, the outwelling where production is either equal to peak biomass (i.e. hypothesis is also applicable to tidal freshwater envi- Dournlele 1981) or biomass adjusted by a mortality or ronments. Ecological simulation (i.e. Buzzelli 1996) or turnover factor (i.e. Pickett 1984, Wohlgemuth 1988, mass balance models (Chalmers et al. 1985, Hopkinson Booth 1989). Few studies have attempted to measure 1988, Anderson et al. 1997) can be used to predict belowground production in tidal freshwater marshes, overall carbon or nitrogen balances in a marsh system, especially those dominated by Peltandra virginica but accurate production estimates must first be ob- which have rhzomes that extend to a depth of 1 to 2 m tained. Sediment microalgae are highly productive (Booth 1989, Chanton et al. 1992).Complete excavation (Sullivan & Moncreiff 1988, Pinckney & Zingmark of belowground material and subsequent separation of 1993),can be suspended and exported from the marsh live and dead roots is a laborious, inexact, and time- by tidal waters (Gallagher 1975), and are often an consuming effort and does not provide necessary in- important food source in aquatic systems (Sullivan & formation on turnover rates. An additional level of Moncreiff 1990, Hamilton et al. 1992, Currin et al. complexity is added because turnover rates for both 1995, Deegan & Garritt 1997). Therefore, any study above and belowground tissues vary depending on the that attempts to couple marsh productivity and food species (Pickett 1984) and tissue type (Schubauer & web dynamics must include sediment microalgae. Hopkinson 1984). In systems dominated by perennial In this study, we describe a carbon gas flux tech- plants, there can be significant translocation of nutri- nique for determining macrophyte and sediment micro- ents and energy from belowground to aboveground algal productivity in tidal freshwater marshes. We components in the spring, and in the reverse direction present estimates of total macrophyte productivity and late in the growing season as aboveground tissues rates of carbon cycling measured using the gas ex- senesce (Lytle & Hull 1980a,b, Hopkinson & Schubauer change technique and compare these with several tra- 1984, Booth 1989). Because translocation is not ac- ditional harvest methods. Additionally, we report the counted for in harvest methods, summing aboveground first known measurements of sediment microalgal pro- and belowground production will not provide an accu- ductivity in a tidal freshwater marsh system. These rate estimate of true macrophyte productivity. data represent a first step in developing coupled car- Neubauer et al.: A carbon gas flux study 15

bon and nitrogen process-based mass balance models ('community chamber', 696 1, Fig. l),as described by for a mid-Atlantic (Virginia) tidal freshwater marsh. Whiting et al. (1992). Belowground metabolism (no aboveground plants) was measured using a smaller chamber ('sediment chamber', 79 cm2, 0.8 1). During MATERIALS AND METHODS spring 1996, 6 alurninum collars for the community chamber were installed along 1 transect and left in Study site. Sweet Hall marsh is an extensive emer- place for the duration of the study. Collars, embedded gent tidal freshwater marsh located on the Pamunkey 10 cm into the sediment, provided an air-tight seal be- River, approximately 69 km from the mouth of the York tween the marsh and community chamber. Holes in River, Virginia, USA. The marsh is within the Chesa- each collar at the sediment surface allowed tidal inun- peake National Estuarine Research Reserve system dation and drainage. Prior to making flux measure- in Virginia (CB-NERRVA),and is bordered by non-tidal ments, drainage holes were plugged; the community hardwood bottomland forests on the mainland side and chamber was clamped to a collar; and the system al- submerged riverine mud flats along the Parnunkey lowed to equilibrate for 10 to 15 min. Sediment cham- River. Nearby upland areas on the Pamunkey River bers were placed adjacent to each community collar. include agricultural fields, mixed hardwood and pine Fluxes were measured during June, September, and forests, and a pine plantation. A tidal and the November 1996 and March, April, May, July, and Sep- Pamunkey River isolate the majority of the marsh from tember 1997. With the exception of the September 1997 direct upland and groundwater influences. study (see below), all measurements were made only Our study site was located along the western branch during daytime low tides. To maximize light intensities of Hill's Ditch, a tidal creek that drains into the Pa- for flux measurements, sampling dates were chosen munkey River on the south end of Sweet Hall marsh. so that slack low water occurred between 11:OO and The tidal range is approximately 80 cm and much of 13:00 h, and sampling did not take place on excessively the marsh is flooded on high tides. The study site (and cloudy or rainy days. Flux measurements in the com- on average, the entire marsh) is dominated by the munity chamber were made in full light and dark and at broadleaf macrophytes Peltandra virginica and Pont- intermediate light levels (using shade cloths; 6 to 7 ederia cordata through most of the summer while the meshes cm-' window screening) in order to construct grass Zizania aquatica becomes abundant late in the photosynthesis versus irradiance curves. Benthic me- growing season. To minimize disturbances due to tabolism was measured only in the light and dark. Flux repeated sampling, 3 boardwalks (30 m) were built measurements at all light levels (including dark) for a into the interior of marsh in May 1996, roughly perpen- given chamber were made on the same day; it gener- dicular to the tidal creek. All sampling was conducted ally took 2 to 3 d to sample all chambers. To maintain from these boardwalks. community chamber temperature at k2"C of ambient, Carbon flux measurements. Marsh community CO2 ice water was pumped through a heat exchanger and CH4 flux studies were performed by enclosing an within the chamber and the headspace air stirred by area of marsh (0.69 m2),including both plants and sedi- 3 fans. The sediment chambers, which were generally ments, within a large temperature-controlled chamber shaded by macrophytes, did not have a cooling system.

Community Chamber (696 1) 16 Mar Ecol Prog Ser

COz concentrations in each chamber were measured sured. Gaseous CO, and CH, fluxes were measured as in the field using a LI-COR model 6252 infrared gas above. For dissolved CH,, 30 m1 water samples were analyzer (IRGA; LI-COR Inc., Lincoln, NE). Prior to shaken for 30 s with an equal volume of CH4-free field measurements, the IRGA was zeroed for 15 to argon in a 60 ml syringe. The gas was transferred to a 30 min with NZpassed sequentially through soda lime 30 m1 syringe with stopcock and analyzed as above (to remove COz),Nafion tubing (Type 815 DuPont per- within 2 d of collection. CH, concentrations in water flourinated polymer, Perma Pure Inc., Toms River, NJ) were calculated using the Ostwald solubility coeffi- packed in silica gel (to remove water) and magnesium cient (0.037 at 20°C, Weiss 1974). Dissolved CO2 con- perchlorate [Mg(C104),,to remove water]. The instru- centrations were not directly measured. Instead, we ment was then calibrated with gas standards contain- assumed that air and water CO2concentrations were in ing 350, 408, or 1000 ppmv CO2 in NZ (Scott Specialty equilibrium, with the concentration of dissolved CO2 Gases, Inc., Plumsteadville, PA). In the field, air was calculated using chamber headspace CO, concentra- circulated (500 ml min-l; LI-COR model 6262-04 refer- tions and the Ostwald solubility coefficient for CO2 ence pump) from the chamber through the IRGA and (0.938 at 20°C, Weiss 1974). Differences in CO2 and back to the chamber; CO2 concentrations were mea- CH4respiration rates due to seasonal, diurnal and tidal sured and recorded at l min intervals using a LI-COR effects were statistically tested using ANOVA and model 1000 datalogger. Five to fifteen measurements Tukey's HSD multiple comparison tests (Zar 1996). were made at each light level. Chamber CO2 concen- Belowground respiration (nitrogen mineralization). trations were always between 280 and 350 ppmv- In freshwater marsh systems, molecular diffusion or preliminary studies in June 1996 indicated that there convective throughflow of sediment gases through was no effect of COz concentration on net photosyn- plant tissues is greater than direct sediment-atmos- thetic rate within this range. phere diffusion (Chanton et al. 1992, Chanton & Whit- To determine CH4 fluxes, 60 ml of gas were with- ing 1996, Whiting & Chanton 1996). Thus, gas fluxes drawn from the community chamber at 10 min inter- measured with sediment chambers may underestimate vals. During November 1996 and September 1997, true belowground. respiration rates (Morris & Whiting samples were also taken from the sediment chamber at 1986). To account for this we used the sediment gross 5 to 7 min intervals. Thirty-five m1 of the sample were nitrogen mineralization rate as a proxy for below- used to flush, and the remainder to pressurize a gas- ground respiration, with N mineralized converted to tight Hungate tube (12.8 ml). Tubes were stored in- carbon units using measured sediment C/N ratios and verted in brine to reduce gas leakage. Upon return to bacterial growth efficiencies (after Linley & Newel1 the lab, 200 p1 samples were injected into a Hewlett 1984, Hart et al. 1994). Although there are potential Packard model 5890 gas chromatograph equipped errors with this approach (see 'Discussion'), we believe with a molecular sieve 13x column and flame ioniza- this estimate will be more accurate than one based tion detector (oven at 80°C, detector at 220°C). A single solely on CO, and CH, efflux into sediment chambers. point calibration of the instrument was performed rou- Gross nitrogen mineralization was determined by tinely before and during analyses using a 9.02 ppmv 15NH4+isotope pool dilution as described in Anderson CH, in NZstandard (Scott Specialty Gases, Inc.). Rates et al. (1997). Sediment cores (10 cm deep) were col- of CH4 flux were linear and showed no response to lected seasonally in triplicate at 5 randomly selected short-term changes in light. points along each transect using polycarbonate core Concurrent with gas flux measurements, incident tubes (20 cm tall X 25.5 cm2).Each core was uniformly irradiance was measured using a LI-COR 2x light sen- injected with 4.0 m1 of argon-sparged 15N-labeled sor placed on top of each chamber, and a 4x sensor ammonium sulfate [(15NH4),S04,10 mM, 99.7 at. %, within the plant canopy, 15 cm above the sediment sur- Isotec Inc., Miamisburg, OH] to an approximate final face. Temperatures were measured using thermistors concentration of 1 mM and 30 at. % 15N in porewater. positioned inside and outside the chamber and in the Cores were incubated at ambient temperature in the sediment (10 to 15 cm). Light and temperature data dark for either 0, 24, and 48 h (November 1996) or 0, 6, were logged at 1 min intervals on a LI-COR model and 24 h (September 1996 and April 1997). After each 1000 datalogger. incubation period, 1 of each set of 3 cores was sacri- Tidal effects on CO2 and CH4 fluxes were deter- ficed by addition of an equal volume of KC1 (255 ml, mined during September 1997. Sampling was con- 2 M) to extract the total exchangeable NH4+pool. Sed- ducted over 1 full tidal cycle, with measurements made iment slurries were shaken in Whirl-Pak bags for 1 h during day and night, on both low and high tides, as on a rotary shaker at room temperature and cen- described above. When the marsh was flooded, CO2 trifuged. Supernatants were filter sterilized (0.45 m and CH, fluxes in the chamber headspace and concen- Gelman Supor Acrodiscs) and stored frozen in Whirl- trations of dissolved CH, in overlying water were mea- Pak bags until analyzed for NH4+using the technique Neubauer et al.: A carbon gas flux study 17

of Solorzano (1969). Remaining supernatants were late productivity. Because different species have their transferred to sterile, disposable specimen cups. Mag- peak biomass at different times of the year, multiple nesium oxide (MgO, 0.2 g) was added to reduce harvests allow a better estimation of aboveground pro- NH4+(,,, to NH3(,, which was trapped on acidified ductivity than does a single harvest. Smalley produc- (KHS04, 10 pl, 2.5 M) paper filters (Whatman #3, tion was calculated by taking into account changes in 7 mm) for 6 d, as described by Brooks et al. (1989). both the live and combined dying plus dead fractions Disks were dried overnight in a desiccator over con- of biomass for all species over the course of the year centrated sulfuric acid (H2SO4),wrapped in tin cap- (Smalley 1958). To account for leaf mortality and de- sules, and analyzed for %N and I5N enrichment using composition between sampling dates,. we applied a an elemental analyzer coupled to an isotope ratio mass turnover factor of 2.24 yr-l (Wohlgemuth 1988) to our spectrometer at the University of California at Davis. estimates obtained from each method. Seasonal trends Rates of N mineralization were determined using a in live, dead, and total biomass were analyzed using model described by Wessel & Tietema (1992) which l-way ANOVA followed by Tukey's HSD multiple takes into account both the change in at. % enrichment comparison tests. of the 15N-labeled NH4+pool as well as the change in Sediment chlorophyll a. For analysis of sediment mi- total concentration of the NH4+pool. croalgal biomass, sediment was collected using 2 cm di- Sediment characterization. Sediment cores (55 cm2 ameter core tubes to a depth of at least 1 cm. Triplicate X 30 cm deep) were collected seasonally and sectioned cores were taken from the same areas sampled for into 0-2, 2-5, 10-13, 18-21, and 27-30 cm intervals. macrophyte biomass, plugged with rubber stoppers, and Samples were dried at 50°C for 3 to 4 wk. A portion of stored in the dark until processed. The 0 to 5 mm section each sample was ground in a Wiley mill (#40 screen), of each core was removed and stored frozen. Analysis weighed into ashed silver cups and acidified with 1 to was performed according to the protocol of Lorenzen 2 drops of 10% HCI to remove carbonates. Samples (1967),as modified by Pinckney et al. (1994)to include were placed on a hot plate to evaporate excess acid, extraction of the sediment (unground) with 10 m1 of The acidification step was repeated and samples extractant (45% methanol, 45 % acetone, 10 % D1 water) allowed to dry overnight in a 50°C drying oven. Total at -15OC for'j2 h. Differences in monthly chlorophyll carbon and nitrogen were measured using a Fison concentrations were analyzed using ANOVA and Tu- model EA 1108 elemental analyzer. key's HSD multiple comparison tests. Aboveground macrophyte biomass. Seasonally, aboveground macrophyte biomass was clipped at 5 points along each of 2 transects in the marsh. Each RESULTS AND CALCULATIONS transect was divided into 5 zones (0-2, 2-8, 8-15, 15-23, and 23-30 m from the tidal creek) and a sam- Carbon flux measurements pling point within each zone was randomly selected. The 2 zones nearest the creek covered the front and Mean short-term community CO2 respiration mea- back sides, respectively, of a natural levee, while the 3 sured as dark CO2 flux (CR; see Table l for abbrevia- interior zones were slightly lower in elevation. A 0.11 m2 tions) ranged from a low of 0.28 mg C m-' min-l in ring was blindly dropped at each sampling point; all March 1997 to a high of 6.51 mg C m-' min-' in Sep- vegetation rooted within the ring was clipped and returned to the lab for sorting. Samples were sorted by Table 1. List of abbreviations used throughout this paper species into living (50 to 100% green), dying (0 to 50 % green), and Units dead fractions, dried at 50°C for 3 to GCp Gross community photosynthesis Mass C m-' per unit time 4 wk, and weighed. Percents carbon Gross macrophyte photosynthesis Mass C m-' per unit time and nitrogen were measured as GMiP Gross microalgal photosynthesis Mass C m-' per unit time above without the acidification TCR Total community respiration (CO2+ CH4) Mass C m-' per unit time steps. From these data, aboveground Community respiration (CO2only) Mass C m-' per unit time ME Community respiration (CH4 only) Mass C m-' per unit time macrophyte productivity was esti- BGR Belowground respiration Mass C m-' per unit time mated using the peak biomass (i.e. M,R Macrophyte respiration Mass C m-' per unit time Whigham et al. 1978, Doumlele MiR Microalgal respiration Mass C m-' per unit time 1981) and Smalley (1958) harvest Gross sediment nitrogen mineralization Mass N m-' per unit time methods. The peak aboveground AGB Aboveground macrophyte biomass Mass C m-' or g dw m-' BGE Bacterial growth efficiency % biomass (converted to g C m-') of MOM Sedunent macro-organic matter - each species was summed to calcu- 18 Mar Ecol Prog Ser 199: 13-30, 2000

tember 1997 (Fig. 2). CR was highest during the sum- Table 2) and lowest in November (0.4 mg N m-' h-'). mer when temperatures and aboveground macrophyte Average sediment C/N ratios in the upper 30 cm biomass (AGB) were greatest. While there was consid- ranged from 11.6 to 12.1. Mineralization, the reduction erable variability between sampling sites on any given of organic matter to NH4+,is largely confined to the live day, average community CH4flwes (ME) were highest root zone. Our data indicate that sediment organic in September 1996 (0.54 mg C m-' min-l) and lowest matter concentrations were fairly uniform (average during April 1997 (0.16 mg C m-' min-l; Fig. 2). Sedi- 19.6 % * 7.0 SD; n = 294) through the top 30 cm of sed- ment CH4 flwes were a small percentage (generally iment. The hlgh standard deviation reflects occasional <5%) of the total ME flw (data not shown). Commu- high organic matter concentrations (50 to 80 %) in the nity ME rates accounted for 5 (May, June 1996; Sep- upper 2 cm. In Peltandra virginica marshes, the highest tember 1997) to 46% (March 1997) of short-term total organic matter content and root concentrations are community respiration (TCR; CR + ME; Fig. 2). TCR observed in the upper 30 cm (Booth 1989, Chambers & followed the same general trend as CR: rates were Fourqurean 1991, Hussey & Odum 1992, Harvey et al. highest between May and September, and signifi- 1995), although live roots and high concentrations of cantly lower from November to April (Fig. 2; ANOVA, sediment organic matter (15 to 20 %) can be present to F= 18.09, p < 0.0001; Tukey's HSD, p < 0.05). depths greater than 1 m (Booth 1989, S.C.N. unpubl.). During September 1997, studies were conducted over In our calculations, we extrapolated our measured 1 full tidal cycle. Mean CR ranged from 4.02 (nighttime rates of N mineralizatidn (to; 10 cm) to 30 cm depth. high tide) to 9.00 mg C m-' rnin-' (nighttime low), but there were no statistical differences in CR over the tidal cycle (Fig. 3A; ANOVA, F=2.68, p = 0.14). In contrast, Aboveground macrophyte biomass and sediment there were large changes in ME over the tidal cycle chlorophyll a (Fig. 3A).All treatments (nighttime low, nighttime high, daytime high) were significantly different than ME There was considerable variability in aboveground measured during daytune low tides (ANOVA,F= 18.18, biomass (AGB) along each transect with highest live bio- p < 0.01; Tukey's HSD, p < 0.05). ME was higher during mass observed near the tidal creek. All sampling loca- the day than at night, and low tide release rates were tions were generally dominated by Peltandra virginica higher than when the marsh was flooded. Gross photo- and Pontedena cordata, with Zizania aquatica increas- synthesis also varied with the tidal cycle (Fig. 3B). ing in abundance at the end of the growing season. Live biomass was highest during May and June and lowest in November (Fig. 4; ANOVA, F = 25.63, p < 0.0001; Belowground respiration (N mineralization) Tukey's HSD, p < 0.05). AGB was not measured during winter when few standing stems were observed. Dead Gross N mineralization in the upper 10 cm of the and dying biomass peaked in July (ANOVA, F = 6.84, sediment was highest in September (20 mg N m-' h-'; p < 0.001; Tukey's HSD, p < 0.01); nearly 70 % of this ma- terial was P. virginica or l? cordata, while 20 % was unidentifiable detritus or wrack. Macro- Community CO2 Respiration phyte C/N ratios ranged from 11.5 (P. cordata, Community CH4 Respiration June) to 26.0 (Z. aquatica, November) and Chamber Temperature increased during the growing season. Sedi- p ment chlorophyll a concentrations in the top 5 mm were highest in May (Fig. 4; ANOVA, F=19.35, p < 0.0001; Tukey's HSD, p < 0.01).

GASEOUS CARBON FLUX MODEL

As a first step in constructing coupled car- bon and nitrogen process-based mass bal- ance models for Sweet Hall marsh, we devel- oped a carbon gas flux model to determine Jun 96 Sep 96 Nov 96 Mar 97 Apr 97 May 97 Ju197 Sep 97 annual rates of macrophyte and microalgal Fig. 2. Seasonal community CO2and CH, fluxes (mg C m-' min-l), and air fixation' and community and temperature within the chamber. Bars are additive; thus combined CO2 + ground respiration. To do this, it was neces- CH, flux = TCR. Error bars are * 1 standard deviation; n = 3 to 7 sary to scale our short-term field measure- Neubauer et al.: A carbon gas flux study 19

I o High Tide 1

..,....,..,.I.~~.I...~j Day Night Night Day 0 500 1000 1500 2000 2500 Low High Low High Incident Irradiance (pE m-' sec-') Tide Stage

Fig. 3. (A) Community CO, and CH4 respiration (mg C m-' min-') measured in darkened community chamber over 1 tidal cycle in September 1997. Error bars are * 1 standard deviation; n = 2 or 3. (B) Gross community photosynthesis versus incident irradiance at high and low tides. Each data point is the slope of CO, concentration versus time for a 5 to 10 min sampling interval, minus measured dark respiration

Table 2. Sediment carbon mineralization rates as calculated from measured gross nitrogen mineralization rates, Cmratios, and estimates of bacterial growth efficiency (BGE). Rates were measured in April, September, and November and extrapolated to seasons as defined below. All rates integrated through the upper 30 cm of the sediment column. n = 16 to 30 for mineralization rates; n = 9 to 29 for sediment C/N

Season No. of days N mineralization Sedvnent C mineralization (g C m-, season-') (mg N m-' h-') Cm BGE = 0.5 BGE = 0.4 BGE = 0.3

P P 'Growth' (Mar to Jul) 153 11.32 11.66a 243b 291 340 'Senescence' (Aug to Oct) 92 20.01 12.06 266 320 373 'Winter' (Nov to Feb) 120 0.43 11.60 7 9 10 Annual totals (g C m-' yr-l) 516 620 723 aSediment C/N values are averages of seasonal C/N values for 0-2, 2-5, 10-13, 18-21, and 27-30 cm sediment sections bCalculated by multiplying N mineralization X number of hours per season X sediment CmX (1 - BGE) ments of community and sediment CO2 and 900, CH., fluxes to daily, monthly, and annual 800 rates. Our model is driven by these seasonal rates, which, in turn, are controlled by hourly g 700; changes in irradiance and temperature (mea- B 600: sured at the Virginia Institute of Marine Sci- 2 , : ence, VIMS, -50 km from Sweet Hall; VIMS !'E 1997) and predicted tidal inundation of the 5 $,400i marsh (modeled with a sine curve; 12 to 13 h . flooding d-l). 5B 300; Carbon flwes were estimated for the 2 yr 200: period from January 1996 through the end of g December 1997. For the model, we made the loo{ assumption that photosynthesis versus irradi- ance (Pvs I) and respiration versus tempera- Jun96 Sep 96 Nov 96 Apr 97 May 97 Jul97 (Rvs T, (see did not Fig. 4. Seasonal patterns of aboveground macrophyte biomass (g dw m-') change from Year to year. Thus, interannual and sedunent microalgal chlorophyll (pg cm-'). Error bars are * 1 standard variations in modeled carbon fluxes are pri- deviation; n = 10 for macrophyte biomass; n = 30 for sediment chlorophyll 20 Mar Ecol Prog Ser 199: 13-30, 2000

manly due to changes in incident irradiance and tem- the entire month of September 1997 (hypothetically perature. For months where field data were not col- assuming the marsh was always flooded or always lected, flux rates were estimated by linear interpolation. dry), there was only a small difference between calcu- lated monthly high and low tide GCP (106 vs 108 g C m-' mo-l, respectively). Therefore, we assumed that Model construction and assumptions there was no change in GCP due to tidal flooding.

Gross community photosynthesis Gross microalgal photosynthesis Measurements of gross community photosynthesis (GCP) were made during 8 mo of the 2 yr modeling per- Because of a lack of low light intensity measure- iod, with data collected at a range of light levels (dark ments during field studies (less than 200 pE m-' s-'), to full light) in each season. GCP was calculated from gross microalgal photosynthesis (GMiP) versus I curves field measurements of net community photosynthesis could not be developed. To scale short-term rates to (light and shaded CO2 fluxes) plus community respira- daily and monthly fluxes, we assumed maximum GMiP tion (CR; dark CO2 fluxes) taken immediately follow- at irradiances greater than 500 pE m-2 S-'. Between ing the light measurements. To determine changes in 0 and 500 pE m-' S-', there was a linear increase from GCP over the course of a day or month in response to 0 to full GMiP. Holmes & Mahall (1982) showed that changing light levels, GCP versus irradiance (I)curves net CO2 exchanges for water-saturated intertidal se- were developed. Data from 6 chambers, placed along a diment~from California plateaued between 500 and transect extending from creekbank to marsh interior 750 pE m-' S-'. Similarly, Darley et al. (1981) observed were used to generate a GCP versus I curve for each saturating irradiances in a Spartina alterniflora marsh season. Hyperbolic curves (after Whiting et al. 1992) of 500 pE m-2 S-' during summer and 100 pE m-' S-' in were fit to the data using the Levenberg- Marquardt iterative method (Deltapoint 1996). Hourly GCP was modeled as: .- 2.0 m C ..Pt ..Pt = [E] 2 1.5 9 7 where GCP, is calculated gross community .z .FE1.0 photosynthesis (mg C m-' h-'); I is average C hourly incident irradiance measured at VIMS 5 t 5 .E (pE m-' S-'); and a and b are empirically U 0.5 derived constants with units of mg C m-' h-' % and pE m-' rl,respectively Hourly GCP, g 0.0 rates were summed to determine daily and monthly fluxes. Incident Irradiance (pE m-' sec-') When data for individual chambers were analyzed, ambient irradiance and GCP were 18 highly correlated (i.e. r2 = 0.84 to 1.00 for l6 April 1997; Fig. 5A). However, when a 14 month's data for all chambers were pooled g 7, 12 (Fig. 5A), the correlation coefficient dropped 5: 10 considerably (r2= 0.30 for April 1997 to 0.88 .z E 8 for ~uly1997), reflecting variability in AGB t 6 g .E and species composition along the transect. U In spite of this, aggregated GCP versus I 3 curves for each month were used to model g 0 the integrated response of the entire, spa- 0 500 1000 1500 2000 2500 tially variable, marsh community to chang- Incident Irradiance (pE m-' sec-') ing light conditions (Fig. 5B). curvesof GCP versus I measured under Fig. 5. (A) Relationship between incident irradiance (I) and gross com- munity photosynthesis (GCP) for April 1997, showing strong correlation and non-f1ooded conditions were for individual chambers, but much lower correlation when all chambers markedly different(Fig. 3B). when are considered. (B) Representative GCP versus I curves used in carbon these curves were used to calculate GCP for gas flux model Neubauer et al.: A carbon gas flux study 21

winter. Whitney & Darley (1983) and Pinckney (1994) throughout a month. The tidal effects study indicated reported saturating irradiances ranging from 500 to that there were significant differences in ME over a greater than 1000 pE m-' S-', depending on the habitat tidal cycle (Fig. 3; ANOVA, F= 18.18, p < 0.01; Tukey's (i.e. creekbank vs marsh interior). Short-term GMiP HSD, p < 0.05). Nighttime rates were 50% of daytime rates were multiplied by 60 to obtain hourly rates rates, suggesting that a light-dependent process was which were then summed to determine daily and responsible for some of the CH, transport. For modeling monthly rates. purposes, night was defined as any time when average In our tidal inundation study, we were unable to hourly irradiance was less than 50 pE m-' S-'. Rates at calculate GMiP during high tide. Using the data of high tide were only 12% of corresponding low tide Holmes & Mahall (1982),wecalculated that gross CO2 rates. Hourly rates of CH, release were calculated as: uptake rates decreased by an average of 49% when MEt = MEi X (0.50)' X (0.12)' the sediments were flooded with only a few mm of water. Pinckney & Zingmark (1993) calculated that where ME, is calculated CH, release rate (mg C m-' microalgal production decreased by less than 25% h-'); MEi is average ME rate during season i (mg C m-' during periods of flooding. To be conservative, we h-'); and the factors 0.5 and 0.12 are added ('as applied the 49% relative decrease from Holmes & needed) to convert daytime low tide rates in response Mahall (1982) to simulate a depression in Sweet Hall to diurnal or tidal changes, respectively. Hourly rates GMiP rates due to increased light attenuation and ver- were summed to obtain daily and monthly fluxes. tical migration (downward) of microalgae during tidal flooding (Pinckney & Zingmark 1993, Pinckney 1994). When modeling tidal effects on carbon flux rates, we Belowground respiration assumed that the depth of water overlying the marsh did not affect process rates; the important factor was Gross N mineralization (GNM) rates measured in whether the marsh was 'wet' or 'dry'. April, September, and November were integrated over a sediment depth of 30 cm. Rates of GNM were con- verted to carbon units using sediment C/N ratios and Community respiration estimated bacterial growth efficiencies (BGE, or micro- bial growth yield) of 30 to 50 % (Linley & Newel1 1984, In April, July and September, Qlovalues were calcu- Hart et al. 1994): lated from plots of respiration versus air temperature Belowground C respiration = (C&)subsbate X GNM X (1- BGE) (CR vs T).Values ranged from 1.94 (July) to 3.2 (April). In other months there was not a significant CR versus T To convert rates from discrete seasons to an annual relationship; so values from April, July or September rate, seasons were defined based on vegetation pro- were substituted based on similarities in overall vege- cesses. Early spring to summer (March to June) was tation characteristics (AGB and species composition). defined as the 'growth' period since AGB rises from Monthly Qlo values were combined with hourly near 0 in March to maximum values in mid-June. weather data measured at VIMS and average monthly Large amounts of Peltandra virginica and Pontederia respiration rates to calculate hourly CR rates: cordata biomass begin to die in July (Fig. 4), and total community AGB continues to decline through the end of the growing season. Thus, July to September was where CR, is calculated hourly respiration (mg C m-2 classified as the period of 'senescence'. From Novem- h-'); CRi is the average CR rate during season I (mg C ber to February ('winter'), AGB was near 0. Within a h-I ); Qlovaries seasonally; and t, and ti are air tem- season, no corrections were made for changes in sedi- peratures ("C) at time t and the time the field measure- ment temperature. ments were made, respectively. There were no tidal effects on CR (Fig. 3; ANOVA, F=2.68, p = 0.14).Res- piration was calculated 24 h d-l; hourly rates were Model results summed to obtain daily and monthly CR rates. Photosynthesis

Methane release Total gross community photosynthesis (GCP) aver- aged 1062 (? 102 SD) g C m-' yr-' over the 1996 to 1997 Community CH, release (ME) was not significantly model period. Results from the sediment chambers show related to either air or sediment temperature; thus we that 66 (+ 12 SD) g C m-' yr-' were fixed by sediment assumed that the rates we measured were applicable microalgae (GMiP). By difference, the remaining 996 22 Mar Ecol Prog Ser 199: 13-30, 2000

(+ 114 SD) g C m-' yr-' was gross macrophyte photosyn- Although not the focus of this paper, we hypothe- thesis (GMaP). GCP was low during winter and early size that sedimentation during tidal flooding provided spring, but increased from 26 to 174 g C m-' mo-' sufficient carbon to the marsh to account for the high between April and May (Fig. 6). This large increase in respiration rates and maintain rates of marsh surface GCP was reflected in the large accumulation of AGB accretion. Alternately, if GCP and TCR vary annually during the same period (Fig. 4), although measured pho- and are out of phase, high autotrophic production in tosynthetic rates were not sufficient to explain the entire 1 yr might not be decomposed until the following year biomass accumulation (see 'Discussion').Following a ma- leading to an imbalance between GCP and TCR. Total ximum in June, and coincident with decreases in AGB, community respiration rates were significantly greater there was a steady decline in GCP through the end of the during the summer (p < 0.05; May to September) than growing season. GCP rates during winter were relatively during the remainder of the year. Of the community constant (12 to 14 g C m-2mo-'), reflecting low AGB dur- respiratory flux, 6% (72 + 4 g C m-2 yr-') was due to ing this time. Statistically, GCP rates were significantly CH4 release (ME);the remaining 94 % (1197 + 134 g C higher (p < 0.05) during the summer (May to September) m-' yr-') was CO2 efflux (CR). CR rates were highest than during the rest of the year (November to April). during July (285 g C m-' mo-l; Fig. 6), perhaps due to Highest GMiP rates occurred in May (14.3 g C m-' mo-l), the large amount of dead and dying Peltandra vir- before the growth of dense macrophyte biomass re- ginica and Pontederia cordata biomass (Fig. 4). ME stricted light penetration to the sediment surface. In rates were highest during the late growing season June, GMiP rates were the lowest of the yr (2.1g C m-' (August to September; 8.4 to 8.6 g C m-z mo-l). mo-'; Fig. 6). GMiP rates again increased toward the end When hourly N mineralization rates were extrapo- of the growing season, possibly due to senescence of the lated to seasonal rates and converted to carbon units dense Peltandra virginica and Pontedena cordata cover using measured sediment C/N ratios and bacterial and subsequent replacement by the tall, thin grass Ziza- growth efficiencies (BGE) ranging from 0.3 to 0.5, nia aquatica, which allowed more light to reach the 'growth' and 'senescence' periods accounted for nearly sediment surface. equal amounts of belowground respiration (BGR; 243 to 340 and 266 to 373 g C m-' season-', respectively; Table 2). Although 'winter' accounted for 120 d of the yr, Respiration BGR during this season (7 to 10 g C m-z season-') was less than 2 % of the annual total. Total community carbon respiration (TCR; CR + ME) Total BGR estimated from sediment nitrogen miner- exceeded GCP, 1269 (* 130 SD) versus 1062 g C m-z yr-l. alization was 516 to 723 g C m-' yr-'. In contrast, carbon respiration (COz + CH4) mea- sured using sediment chambers was 75 300 l Photosynthesis 7300(* 2 SD) g C m-2 yr-l, suggesting that over 85 % of COz and CH4produced in _-200 200 the sediments was transported through 5 macrophytes before being released to E 100 100 P! the atmosphere. Methane release (72 g E U C m-' yr-l) accounted for 11 to 13 % of ,M 0 0 total BGR. However, nearly all CH4 X z passed through plant tissues-sedi- U h 100 100 ment CH4 fluxes were generally

300 300 release due to methane oxidation in Jan Feb Mar Apr May Jun lul Aug Sep Oct Nov Dec the sediment (Yavitt 1997), gas trans- port through plant stems appears to Gross Microalgal Photosynthesis (GMiP) Community COz Respiration (CR) provide a more efficient mechanism of Gross Macrophyte Photosynthesis (GMaP) Community CH4 Respiration (ME) releasing CH4 to the atmosphere than + Gross Community Photosynthesis (GCP) + Total Community Respiration (TCR) direct sediment-atmosphere diffusion. The difference between TCR and Fig. 6. Monthly rates of gross macrophyte and microalgal photosynthesis and community CO2 and CH4 respiration (g C m-' mo-') from carbon gas flux model. BGR (546 to 753 g C m-z yr-l) can be Values are averages of 1996 and 1997 model output (i 1 standard deviation; divided among marsh macrophyte and error bars do not include prediction error of the P vs I or R vs T regressions) microalgal respiration (MaR and MiR, Neubauer et al.:A carbon gas flux study 23

respectively). Pomeroy (1959) stated that MiR was less calculated to range from 536 to 715 g C m-2 p-' (Z= than 10% of GMiP. Using this value, we calculated a 625 g C m-2 p-').Based on studies by Hwang & Morris MiR rate of 7 g C m-2 yr-' and a net microalgal photo- (1992) in a Spartina alterniflora marsh, 5 to 37 g C m-2 synthesis rate of 60 (* 10) g C m-2 yr-'. This wiU under- yr-' (F = 21 g C m-2 yr-') were fixed via DIC uptake by estimate total microalgal production to the extent that the roots (0.5 to 3.7 % of GMaP). Therefore, net macro- the algae utilize porewater DIC in addition to atmos- phyte production (net photosynthesis + DIC uptake) pheric CO2. The remaining 539 to 747 g C m-2 p-' of was 557 to 736 g C m-2 (5f = 646 g C m-2; Fig. 7). respiration was due to macrophyte growth and respira- Early summer translocation of carbon from below- tion costs and decomposition. ground rhizomes to aboveground tissue is critical to support accumulation of aboveground biomass (AGB). Production of peak AGB required a total of 676 g C m-2 Macrophyte carbon budget between the start of the growing season (March) and the time of peak biomass (June; calculated from peak On an annual basis, 996 g C m-2 yr-' (Table 3) were AGB, species-specific % carbon values, and a turnover fixed by marsh macrophytes (GMaP).During the early of 2.24 yr-l). During this 4 mo period, net photosyn- growing season (March to June), there was little de- thesis accounted for only 35 to 45% of the carbon caying AGB (Fig. 4); therefore, measured TCR inclu- required. The remaining 367 to 444 g C m-2 (F = 405 g ded MaR necessary for growth and maintenance and C m-2) was likely supplied by translocation from below BGR. MaR, calculated as TCR - BGR - MiR, was sub- to aboveground tissues. Following peak biomass, AGB tracted from GMaP to give a net macrophyte photo- disappeared from the surface of the marsh. Possible synthesis rate of 232 to 309 g C m-2 (F = 271 g C m-2; fates include respiration to CO2 or CH,, leaching as March to June only). As the growing season progres- DOC during tidal flooding, translocation to below- ses, decomposition of AGB makes up an increasing ground tissues, and other losses which include her- proportion of TCR. To calculate MaR while accounting bivory, deposition on the sediment surface or export for decomposition, we assumed that growth and main- from the marsh. Using our carbon gas flux model, some tenance respiration costs were a constant percentage literature values, and a few simplifying assumptions, of GMaP, regardless of the time of year. During March we have completed a conceptual carbon flux model, to June, we calculated that macrophyte respiration was described below, for macrophytes in Peltandra virgi- 28 to 46% of GMaP. Based on thls estimate, MaR for nica dominated tidal freshwater marshes (Fig. 7). the remainder of the yr would range from 159 to 261 g Leaching of DOC from plant tissues can occur both C m-' yr-' (F = 210); the remaining 259 to 287 g C m-2 during tidal submergence and aerial exposure (Gal- (F = 273 g C m-2) would result from plant decomposi- lagher et al. 1976, Turner 1978, Pakulski 1986, Moran & tion. Annual net macrophyte photosynthesis was thus Hodson 1990, Turner 1993, Mann & Wetzel 1996).

Table 3. Model output and sensitivity analysis for conceptual carbon flux model (Fig. 7). Case 1 to 3: variations in the bacterial growth efficiency from 30 to 50%. Cases 4 and 5: variations in the ratio of (MaR) macrophyte respiration to (GMaP) gross macrophyte photosynthesis. Units are g C m-2 yr-'

Case 1 Case 2 Case 3 Case 4 Case 5 Bacterial growth efficiency (%) MaRIGMaP (%) 50 4 0 30 40 5 0 System gas flues Gross macrophyte photosynthesis 996 996 996 996 996 Macrophyte respiration 459 370 28 1 3 98 497 Macrophyte decomposition 287 273 '259 277 293 Macrophyte respiration/gross photosynthesis (%) 46 37 28 4 0 50 Belowground respiration 516 620 723 587 472 Carbon inputs Net macrophyte photosynthesis 536 625 715 597 498 DIC uptake 21 21 2 1 21 21 Internal cycling Spring translocation 444 405 367 4 17 46 1 Autumn translocation 460 460 460 460 460 Carbon outputs Dissolved losses (leachingterms) 66 66 66 66 66 Particulate losses ('other losses') 204 307 410 275 160 Maximum C for export (dissolved plus particulate) 270 374 477 34 1 226 24 Mar Ecol Prog Ser

Total loss of root matter during the early growing sea- son (March to June) was 474 g C m-'. Of this, 33 to 110 g C m-' (X = 72 g C m-') were transferred from belowground biomass to the sediment MOM pool (474 g C m-' total loss - 367 to 444 g C m-' transloca- tion loss - 3 g C m-' leaching loss + 7 g C m-' DIC uptake), although the ultimate fate (e.g. respiration to CO2 and CH4, export from the marsh) of this MOM is unclear. Because belowground biomass standing stocks are similar at the beginning and end of the year (Booth 1989), we balanced all inputs to the below- ground compartment (DIC uptake and fall transloca- tion) with outputs (leaching, spring translocation, and other losses) to calculate an autumn translocation rate of 460 g C m-' yr-t. Similarly, we balanced all inputs and outputs from the aboveground compartment (as- Other losses suming that AGB is 0 at the beginning and end of the year) and determined that 171 to 300 g C m-' yr-' (X = DIC Uptake 235 g C m-') of AGB was lost by herbivory, detritus deposition on the sediment surface, or export from the Fig. 7. Conceptual model of carbon fluxes in a Peltandra marsh by tidal waters. The partitioning between these virginica dominated tidal freshwater marsh. Bacterial growth loss terms is currently unknown. efficiencies from 30 to 50% were used in the calculations presented in the text. For visual simplicity, only results using a median efficiency of 40% are shown here. Units are g C m-'yr-' DISCUSSION

The gas exchange technique described herein pro- Working in Spartina alterniflora salt marshes, Turner vides a non-destructive means of determining total (1993) calculated that 5 to 10% of total aboveground macrophyte and microalgal production. Because pro- production was leached from plant tissues. From our duction numbers are based on actual process model- biomass harvests, seasonal and species-specific percent ing, a relatively large amount of data (e.g. GCP vs I, CR carbon data, and an annual live biomass turnover vs T curves) are needed to construct a robust model. of 2.24 yr-' (Wohlgemuth 1988), we calculated above- Additionally, there are a series of assumptions (see ground productivities using the peak biomass (845 g C 'Gaseous carbon flux model') that must be made to m-2 yr-l) and Smalley methods (776 g C m-' yr-L).Com- successfully extrapolate short-term (5 to 30 min) field bined with Turner's (1993) data, we estimated a leach- measurements to monthly and annual budgets. How- ing rate of 41 to 85 g C m-2 yr-' (F = 62 g C m-' yr-'). ever, if these process relationships can be described Using Booth's (1989) nitrogen leaching rates for Peltan- and all assumptions confidently justified, a gas flux dra virginica and a C/N ratio of 16.3 for aboveground modeling approach can provide a degree of process- tissues (this study), 34 g C m-' yr-I were leached from related insight into differences in primary productivity aboveground tissues. Both of these values are likely over the course of several years or between different underestimates of true leaching rates as S, alterniflora marshes in the same year. is more resistant to degradation than fleshy plants like P. virginica (Odum & Heywood 1978, Webster & Ben- field 1986),and Booth's (1989) study examined only live Gas exchange technique versus harvest methods standing leaves; leaching rates are higher from dead and dying tissues (Mann & Wetzel 1996). Annual net macrophyte production (557 to 736 g C m-' We assumed that DIC uptake occurred at a constant ~r-')determined using our gas flux model was lower rate of 1.75 g C m-2 mo-', for an annual total of 21 g C than that based on AGB harvest methods (776 to 845 g C m-2. Belowground leaching rates (4 g C m-' yr-t)were m-2 yr-l) adjusted by a turnover rate of 2.24 yr-' (Wohl- estimated from Rovira (1969) who reported that root gemuth 1988). As previously discussed, harvest tech- leaching rates from a range of species are rarely more niques tend to bias production estimates by failing to than 0.4 % of GMaP. Combined root and rhizome mor- account for seasonal translocation while the gas ex- tality (defined here as loss to sediment macro-organic change technique implicitly includes translocation and matter, MOM) was estimated based on Booth (1989). biomass turnover in production calculations. Neubauer et al.: A carbon gas flux study 25

Several studies have measured both aboveground (Table 4). Estimates from a Spartina alterniilora salt macrophyte biomass and production in tidal freshwa- marsh show that, given the assumptions and limita- ter marshes (Fig. 8). Because there is a wide range in tions inherent in each approach, the gas exchange and aboveground productivity depending on marsh spe- ecophysiological techniques provide similar produc- cies composition (Whigham et al. 1978),we limited our tion rates (Anderson et al. 1997). comparison to Peltandra virginica and Pontederia cor- data, the 2 dominant species at our study site. In order to compare annual production values, we converted Nitrogen mineralization literature production values from g dw m-' yr-' to g C m-' yr-' assuming a percent carbon of 48.5 % (our data, In spite of the uncertainties associated with using N P. virginica, June). Our values of peak aboveground mineralization rates to calculate belowground C respi- biomass fall within the wide range of values reported ration, we believe that this method is more accurate for other east coast P. virginica and P. cordata domi- than directly measuring CO2and CH4 gas efflwes into nated tidal freshwater marshes (Fig. 8), while our sediment chambers. Few studies have simultaneously annual production is among the highest reported. This measured both carbon respiration and gross nitrogen reflects the high biomass at our site, but also indicates mineralization; none have done so in tidal marshes. the sensitivity of the production estimate to the as- Worlung in grassland and cropland soils in North sumed rate of biomass turnover. The studies reported Dakota, Schimel (1986) reported no correlation be- in Whigham et al. (1978), Doumlele (1981), and the tween CO2 evolution and gross N mineralization over peak biomass and Smalley methods of Wohlgemuth the course of a 4 d laboratory incubation and attributed (1988) do not account for complete turnover of leaf this to changes in substrate quality (i.e. C/N ratio) material during the growing season. These studies will during the incubation. In contrast, studies in an old- underestimate true macrophyte production as P. vir- growth forest in Oregon (Hart et al. 1994) and a pine ginica leaves can lose up to 50% of their dry weight plantation in New Zealand (Scott et al. 1998) found after only 9 d of immersion (Odurn & Heywood 1978). strong correlations between CO2 evolution and gross The remaining data points on Fig. 8, with the excep- N mineralization rates. Hart et al. (1994) calculated the tion of Booth (1989),fall between the lines indicating a C/N ratio of the respired substrate as 10 to 12, com- turnover (production/peak biomass) of 2 and 2.5 yr-' pared with a C/N ratio of 26.8 for forest soils. This and represent a more accurate estimate of above- difference suggests the presence of 2 sediment organic ground marsh production. pools, one that is labile and rapidly mineralized (i.e. proteins and sugars) and another more recalcitrant pool (i.e. cellulose and lignin). Because emergent marsh Microalgal production macrophytes contain less cellulose and lignin than woody terrestrial plants (Odum & Heywood 1978),the Sediment microalgal production rates measured in C/N ratio of respired marsh organic matter will be sim- this study fall in the wide range of 30 to 200 g C m-' ilar to that of marsh sedirnents. Thus, we converted N yr-' reported for salt marshes and intertidal habitats mineralization rates to C respiration using the C/N

- 1200 L ,h l000 Fig. 8. Aboveground produc- 'E U tion versus peak biomass for g 800 Peltandra virgmica andfor Pon- C tederia cordata only in tidal 0 .M 4 freshwater marshes. Symbols 600 U2 as follows: 0 Whigham et al. ae (1978); O Doumlele (1981); Q Pickett (1984); O Wohlge- 2 400 muth's (1988) peak biomass, 2 @ Smalley, O mortality, and @ F 200 Allen curve methods; O Booth 0 (1989); @ this study's peak bio- 2 mass, and 8 Smalley methods. 0 Lines inhcate turnover (pro- duction/peak biomass) of 1, 2, Peak Aboveground Biomass (gdw m-2) and 2.5 yr-' 26 Mar Ecol Prog Ser 199: 13-30, 2000

ratio of the sediments (11.6 to 12.1). Our measure of bacterial growth efficiency is theoretically no greater belowground respiration (516 to 723 g C m-' yr-l) may then -40%. However, in the presence of available ni- include some root respiration since no attempts were trogen (e.g. DIN) in excess of that present in the sub- made to separate fine roots from the sediment matrix strate, actual growth efficiencies can be greater than prior to the N mineralization studies. the theoretical maximum (Newell et al. 1983, Benner & Based on belowground biomass and sediment organic Hodson 1985, Benner et al. 1988, Bano et al. 1997, del matter profiles for Sweet Hall and other Peltandra vir- Giorgio & Cole 1998). Because fleshy emergent fresh- ginica dominated freshwater marshes, we assumed that water marsh plants are lower in lignin and humic com- mineralization was constant through the top 30 cm of the pounds than salt marsh or woody plants and generally sediment column. Bowden et al. (1991) measured depth have lower C/N ratios, they are degraded more easily profiles of sediment mineralization in peat sediments (Odum & Heywood 1978, Odum et al. 1984, Webster & along the North River, Massachusetts, and observed Benfield 1986) and may be expected to support mi- minimal N production or consumption between 10 and crobial communities with higher growth efficiencies. 30 cm. However, their study location was dominated by Therefore, we used a range of bacterial growth effi- Zizania aquatica, Carexspp., and Typha latifolia-spe- ciencies ranging from 30 to 50% ('theoretical' maxi- cies with relatively shallow root distributions. Bowden et mum * 10 %) to convert sediment N mineralization to C al. (1991) observed a distinct organic matter minimum at respiration. 30 cm; we observed constant concentrations (15 to 20 %) to greater than 1 m. These factors suggest that mineral- ization will occur to a greater depth at Sweet Hall than Model sensitivity analysis observed by Bowden et al. (1991),but this assumption needs to be experimentally verified. However, it is a We performed sensitivity analyses to determine how daunting task to determine mineralization rates over a our conceptual model responds to variations in BGE 1 m sediment profile in an extremely patchy environ- and MaR rates (Table 3). When BGEs used in our analy- ment where rates can be expected to vary both spatially ses were varied from 30 to 50% (cases 1 to 3), calcu- (horizontally and vertically) and temporally. lated BGR varied by over 200 g C m-' yr-l. Although a There are few estimates of BGE on marsh plants or BGE of 30 % (case 3) is most similar to microbial yields sediment organic matter. In the absence of exogenous on plant detritus (del Giorgio & Cole 1998),it may over- nutrient sources, the theoretical maximum microbial estimate the true BGR rate since macrophyte respira- growth yield is equal to the C/N ratio of bacteria tion (281 g C m-2 yr-l) is only 28 % of GMaP. In contrast, divided by the C/N ratio of the substrate (Linley & the ecophysiological model of Dai & Wiegert (1996) cal- Newel1 1984). Assuming a bacterial C/N of 5 and mea- culated total macrophyte respiration rates of 43 to 50% sured sediment C/N ratios for Sweet Hall (11.6 to 12.l), of GMaP for Spartina alterniflora. Because BGR and Neubauer et al.: A carbon gas flux study 27

MaR are directly Linked in our calculations, overesti- m-' yr-l) and the spring translocation of 'recycled' car- mating BGR will underestimate MaR and reduce the bon stored in belowground rhizomes (F = 405 g C m-' apparent respiration/photosynthesis ratio. Alternatively, yr-l; range 367 to 444 g C m-2 F-'). In autumn, a it is possible that the BGR rates in case 3 are accurate slightly larger quantity of carbon (462 g C m-2 F-')is since respiration costs are proportionally higher in salt moved back to belowground tissues as plants senes- marsh than freshwater plants due to salt (Cavalieri & cence, contrasting with N cycling where significantly Huang 1981, Mendelssohn & Burdick 1987) and sulfide greater quantities of nitrogen are translocated above- stresses (King et al. 1982). Cases 4 and 5 forced annual ground in the spring than belowground in the autumn MaR to 40 to 50 % of GMaP (the range reported by Dai (Walker 1981, Hopkinson & Schubauer 1984, Booth & Wiegert 1996) by increasing MaR (rather than by 1989). Presumably this difference reflects the domi- decreasing GMaP). The results from these cases were nant sources of carbon (atmospheric fixation) and similar to those obtained from BGE estimates of 40 and nitrogen (belowground uptake) to the plants. 50%, suggesting that these growth yields are close to We have attempted to examine the fates of net the true values for this system. macrophyte production as a first step in determining To further constrain our results, we estimated rates of the role that these highly productive plants play in sup- GMaP and MaR using leaf-only gas flux measurements. porting detrital or microbially based food webs in adja- In Peltandra virqinica, there is restricted gas transport cent tidal waters. We estimate that 66 g C m-2 yr-' along the length of the petiole (Frye 1989, Chanton et al. (combined above + belowground) are leached from 1992).Instead of passing through leaves, CH4and sedi- standing stems, roots, and rhizomes. This leachate may ment-produced COz diffuse directly from the petioles to be potentially important as a source of DOC to micro- the atmosphere. Therefore, measuring gas fluxes from bial food webs in adjacent tidal waters or it may be leaves provides an independent means of measuring respired in situ and form a portion of measured below- growth and maintenance respiration and partitioning ground respiration. Labile DOC leached from Spartina BGR and MaR. Using mid-summer (July) leaf-only flux alterniflora has been correlated with enhanced rates of rates measured in a mixed Zizania aquatica and P. vir- community respiration in waters adjacent micatidal freshwater marsh on the Edisto River, South to Georgia salt marshes (Turner 1978, Pakulski 1986), Carolina (C. Nietch pers. cornrn.) and Sweet Hall bio- while Mann & Wetzel (1996) demonstrated high rates mass numbers (this study), we calculated an average of bacterial production on leachates from aquatic ma- GMaP rate of 310 g C m-2 (July only) and a leaf respira- crophytes. Thus, marsh macrophytes can contribute to tion rate of 154 g C m-'. These rates were higher than microbially-based food webs in adjacent ecosystems. measured at Sweet Hall using the community chamber The ultimate fate of 204 to 410 g C m-2 yr-' (F= 307 g (Fig. 6). Because photosynthesis and respiration rates are C m-' yr-l; combined above and belowground 'other higher in leaves than in petioles and stems, using leaf- loss' terms) is unknown. These plant tissues are either only flux measurements and total AGB (leaves + stems consumed by herbivores, deposited as detritus on the + petioles) will tend to overestimate rates. With this sediment surface or macro-organic matter in the sedi- approach, MaR was 50 % of gross photosynthesis. For ment matrix, or exported from the marsh as dissolved comparison, using a BGE of 50 % to convert gross sedi- or particulate carbon. With the exception of a couple ment N mineralization to C respiration (Table 3, case 1) of species (notably Hibiscus moscheutos), direct con- we produced a MaR to GMaP ratio of 46 %. The similar- sumption of plant tissues by insects and birds is report- ity of these numbers is additional evidence that our con- edly minimal, accounting for less than 10% of plant version of gross N mineralization to C respiration using production (Odum et al. 1984, Cahoon & Stevenson sediment C/N ratios and BGEs was valid. 1986). The particulate carbon that is not directly con- sumed by herbivores falls to the sediment surface and enters the detrital pool where it contributes to below- Macrophyte carbon budget ground respiration, vertical marsh accretion, or is ex- ported from the system. Interestingly, the relative labil- Our conceptual model of macrophyte-mediated ity (high nitrogen and low cellulose/lignin content) of carbon flows in Peltandra virqinica dominated tidal freshwater marsh macrophyte tissues may limit their freshwater marshes is the first effort of this type. Few importance in aquatic food webs. Utilization of a food studies have attempted to couple aboveground pro- source by a consumer depends not only on the quality ductivity with belowground biomass (translocation of the food item, but also on the availability of that and re-translocation), thereby limiting their utility in a food. If decomposition and leaching are rapid enough larger ecological context. The production of above- to remove detritus (as COz, CH, or DOC) before partic- ground biomass is supported by net macrophyte pho- ulate matter can be exported from the marsh, labile tosynthesis (F = 625 g C m-' yr-l; range 536 to 715 g C detritus may play only a small role in supporting sec- 28 Mar Ecol Prog SE

ondary production (Findlay et al. 1990). Because the Reserve. PhD dissertation, College of William and Mary, partitioning between these fates has important impli- Virginia Institute of Marine Science, Gloucester Point cations in the role of marsh macrophytes as sources of Cahoon DR, Stevenson JC (1986) Production, predation, and decomposition in a low-salinity Hibiscus marsh. Ecology energy and nutrients to riverine food webs, further 67(5):1341-1350 research should address the cycling of carbon both Cammen LM (1991) Annual bacterial production in relation to within tidal freshwater marshes and between these benthic microalgal production and sediment oxygen up- marshes and adjacent ecosystems. take in an intertidal sandflat and an intertidal . Mar Ecol Prog Ser 71:13-25 Cavalieri AJ, Huang AHC (1981) Accumulation of proline and Acknowledgements. Invaluable field and laboratory assis- glycinebetaine in Spartina alterniflora in response to NaCl tance was provided by Betty Berry Neikirk, Mike Campana, and nitrogen in the marsh. Oecologia 49:224-228 Britt Anderson, Yongsik Sin, and Craig Tobias. Ting Dai, Chalmers AG, Wiegert RG, Wolf PL (1985) Carbon balance in VIMS, critically reviewed an early draft of the manuscript, a salt marsh: interactions of diffusive export, tidal deposi- while Chris Nietch, University of South Carolina, graciously tion and rainfall-caused erosion. Estuar Coast Shelf Sci 21: allowed us to use some, of his unpublished data. The com- 757-771 ments of Jeff Cornwell, Jim Morris, and an anonymous Chambers RM, Fourqurean JW (1991) Alternative criteria for reviewer greatly improved the manuscript. Finally, and per- assessing nutrient limitation of a macrophyte haps most importantly, we thank the CB-NERRVA and the (Peltandra virginica (L) Kunth). Aquat Bot 40:305-320 Tacoma Hunt Club for granting us access to Sweet Hall Chanton JP, Whiting GJ (1996) Methane stable isotopic distri- marsh. This research was supported in part by NSF grant butions as indicators of gas transport mechanisms in emer- DEB-9411974 to the University of Virginia, and the Virginia gent aquatic plants. Aquat Bot 54:227-236 Department of Environmental Quality through NOAA grants Chanton JP, Whiting GJ, Showers WJ, Cnll PM (1992)Methane NA570Z0561-01 and NA670Z0360-01. This is contribution no. flux from Peltandra virginica: stable isotope tracing and 2310 of the Virginia Institute of Marine Science, School of chamber effects. Global Biogeochem Cycles 6(1):15-31 Marine Science, College of William and Mary. Colijn F, de Jonge VN (1984) Primary production of micro- phytobenthos in the Ems-Dollard . 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Editorial responsibility: Otto Kinne (Editor), Submitted: May 20, ,l999; Accepted: December 15, 1999 OldendorfLuhe, Germany Proofs received from author(s): June 5, 2000