Passive filtering of microbial biomass by Spartina alterniflora

Estuarine,

Coastal

and Shelf

Science

(1986) 22,545-557

Passive Filtering of Microbial Spartina alternijbra*

Biomass

Thomas

Zingmarkb

H. Chrzanowski”

and Richard

“Department of Biology, The University of Texas at Arlington, TX 76019 and bDepartment of Biology and Belle W. Baruch Biology and Coastal Research, University of South Carolina, SC 29208, U.S.A. Received

Keywords:

3 December

Spartina,

1984 and in revisedform

SJune

Arlington, Institute for Columbia,

by

Marine

198.5

bacteria,estuaries,filtration

Tidal fluctuationsof total microbial biomass(asextractableadenosinetriphosphate, ATP) and phytoplankton biomass(asextractablechlorophyll a, CHL) wereinvestigatedwithin a definedtidal basin,the Bly Creekbasin,in the North Inlet estuarineecosystem(South Carolina, U.S.A.). Sampleswere collected synoptically from a transectacrossBly Creekand from a flume coveringflats of Spartina alterniflora. The samplingdesignallowedfor water to be sampledasit enteredtbe upper basinand, somewhatlater, asit flowed over the grassflats. Tidally induced fluctuations in concentrationdependedupon tide elevation (spring or neap).During springtides, ATP and CHL fluctuated out-of-phase with the tide. During neap tides, concentrationsof ATP and CHL reached maximumlevelson ebbingtide phases.The creekbank areaassociated with tall Spartina appearedto effectively remove microbial biomassfrom the water column. The grassflats also appearto be a location where the suspended microbialassemblages may be separatedinto componentpopulations. Introduction Marsh-estuarine systemsare composedof networks of tidal creeksthat serve aschannels for the movement of suspendedmaterials. There is a considerable literature characterizing the movement of suspended materials in terms of direction and magnitude. The majority of such studies have been concerned with organic carbon flows [see Nixon (1981) for review]. Few studies are available addressing the transport of microbial biomass (Axelrad et al., 1976; Chrzanowski et al., 1982a) or attempting to identify the dynamics of populations involved in the transport process. Tidally induced oscillations of various components comprising the suspended microbial assemblagemay supply insights into dynamics of populations involved in transport processes.Erkenbrecher and Stevenson (1979) thought that receeding tidal waters resuspended bacteria and algae from the marsh surface causing increased concentrations of both populations at low tide. Baillie and Welsh (1980) reported that algae were resuspended asa result of various physical characteristics of flooding and receeding *ContributionNo. 585of the BelleW. BaruchLibrary in MarineBiologyandCoastal Research. 545 0272-9614/86/050545+13$03.00/0

0 1986AcademicPressInc. (London)Limited

546

T. H. Chrzanowski &3 R. Zingmark

water. Chrzanowski et al. (1982b) demonstrated that tidally induced patterns in suspended fungi resulted in greater numbers of propagules during low tide periods and suggested that suspended fungi originated in high-marsh areas and were swept out of the marsh during low tide periods. Stevenson et al. (1981) used resuspended geofungi to demonstrate that water in a marsh system at low tide was pushed back into high-marsh zones by the next flood tide. They additionally suggested that low tide peaks in fungi at marsh-ocean interfaces were indicative of parcels of ‘ marsh water ’ being lost to the ocean on successive low tides. Wilson et al. (1981) used fractional filtration procedures and ATP analysis to show that the composition of the microbial assemblage passing a marsh-ocean interface changed over the course of a tidal cycle. During high tides, the assemblage was dominated by phytoplankton; 79% of extractable ATP originating from this source. During low tide periods, only 33-44% of the total ATP was attributed to phytoplankton; the remaining portion was attributed to bacteria which were thought to be resuspended from the marsh surface. Thus it appears tidal action induced a shift in the structure of the suspended microbial assemblage. In July 1982 and throughout the summer of 1983 tidal fluctuations of total microbial biomass and phytoplankton biomass were investigated in a deiined tidal basin. Tidally induced fluctuations in variables were monitored in the creek at the entrance to the basin as well as at Spartina grass flats in the upper reaches of the marsh within the basin. The data suggested possible mechanisms of coupling between the water column and intertidal regions of marsh that may account for observed dynamics of microbial assemblages described above (Wilson et al., 1981). Materials

and methods

In July 1982 and every 11 days throughout summer and early fall of 1983 tidal characteristics of total microbial biomass (as extractable adenosine triphosphate, ATP) and of phytoplankton biomass (as chlorophyll a, CHL) were investigated in the Bly Creek basin within North Inlet ecosystem near Georgetown, S.C. (33”2O’N, 79”1O’W, Figure 1). Stratigraphic and geomorphic features of the Bly Creek basin have been previously described (Gardner & Bohn, 1980). Samples were collected during day and night conditions from two locations in the basin; from the Spartina grass flats of the upper reaches of the basin (hereafter flume, Figure l), and from a transect across Bly Creek (hereafter transect). The transect was located approximately 1500 m seaward from the flume (Figure 1). During the summer of 1983, samples were collected synoptically at both locations. Synoptic sampling made it possible to follow changes in total microbial biomass and phytoplankton biomass as tidal water entered the upper basin and, somewhat later, as it left the creeks and flowed over the grass flats. Short-term, high-intensity sampling studies (calibration studies) were conducted at both the transect and flume to establish sampling criteria (optimal frequency and depth). Transect sampling and analysis was essentially identical to that described by Kjerfve et al. (1981). The calibration conducted at the flume has been described elsewhere (Wolaver et al., 1985, in press). Grass A flume, 2 m wide and and extended from Bly alterniflora. The flume

flat sample collection 142 m long, was constructed from 0.60 m x 2.4 m fiberglass panels Creek through stands of tall, medium, and short-height Spartina was designed to permit tidal waters to flood and ebb unimpeded

Dynamics of populations

547

N33”

20

LEGEND

I3

q q _

0

300

MARITIME

FOREST

JUNCUS

MARSH

SPARTINA MARSH CA”SEWAY,ROAD

600m

BLY

CREEK LOW

BASIN

WATER

t

N33”

20

LEGEND

v

q

MARITIME

gj

JUNCUS

FOREST MARSH

I3

SPARTINA

-

CAUSEWAY/ROAD

BLY

CREEK

BANKFUL

MARSH

BASIN STAGE

Figure 1. Diagram of the Bly Creek basin, North Inlet Estuary, S.C., showing the approximate position of the transect and marsh flume sampling locations: (a) Bly Creek basin at low tide, (b) at bankfull stage.

but to prevent lateral water movement. The unit was similar to that used by Wolaver et al. (1980) in a Virginia marsh. During 1982 (calibration studies) water was pumped (Master-flex model 7570, Horizon Ecology Co.) at approximately 30 min intervals from various depths within the flume. Bottom (1 cm of?), mid, and surface (5 cm below) samples were collected when the water column exceeded 45 cm. Bottom and surface samples were collected when the water depth exceeded 25 cm. Only one depth was

548

T. H. Chrzanowski

&R.

Zingmark

sampled at other times. During 1983 a similar sampling schemewasused except samples from various depths were collected hourly for a tidal cycle and sampleswere pooled into a single composite sample for each station. Water was collected in sterile, acid-washed, 500-ml glassbottles and rapidly transported in iced coolers to nearby laboratory facilities. Sampling stations were located at the mouth of the flume in tall Spartina, and within medium height Spartina, 27 m landward from the creek. Transect

sample collection

Samples were collected hourly from a single vessel moored in the creek center. Water was collected from bottom and mid-depths by submerging and filling a sterile acidwashed, 500-ml, glass bottle. The sealed bottles were held in a lowering frame that allowed the bottles to be opened and filled at appropriate depths. Sample collections were initiated at low tide and continued for one complete tidal cycle. Samples were periodically transported to nearby laboratory facilities in iced coolers. Analytical

procedures

Total microbial biomass (ATP) was extracted in boiling Tris buffer from subsamples (20ml) filtered through 25-mm glass-fiber filters (Whatman GF/F) (Holm-Hansen & Booth, 1966; Holm-Hansen, 1973). Extractions were done in triplicate and assayedby the luciferin-luciferase technique coupled to an SAI photometer (model 3000) operated in the peak height mode. Mean values from triplicate assayswere used in subsequent computations. Chlorophyll a filtrations were performed in triplicate using 20-ml sub-samples and 25-mm glass-fiber filters (Whatman GF/F). Pigments were extracted in 90% acetone in combination with a freeze-thaw procedure (Glover & Morris, 1979), and measured on a Turner fluorometer (model 111). Mean values from the triplicate extractions were used in subsequent analyses. Results Water depth at the flume mouth was reflective of relative tidal height within the basin. Water depth of 19 cm was necessary to flood the sampling station within tall Spartina whereas water level in excess of 26 cm was necessary before the water depth at the medium Spa&za station was sufhcient to collect samples. Two patterns describe tidally induced fluctuations of ATP and CHL; one typical of spring tides, and the other typical of neap tides. Results presented below are organized by tide phase and sampling location. The standard error of mean concentrations of samplesfrom the transect, was less than 10% of the mean for more than 90% of the samples. Similar results were obtained at the flume for triplicate sub-samplesof pooled samples.Consequently, error bars were omitted from the figures. Spring

tides

Figures 2(a) and 3(a) are examples of changesin tidal height and concentration of ATP and CHL at the transect. Both variables fluctuated out-of-phase with the tide. The maximum level of each variable was obtained at low tide periods. As tide rose from low to high, concentrations of ATP and CHL typically dropped 40 to 70% and 50 to 75%, respectively. The out-of-phase fluctuation pattern was more pronounced in early summer and fall than in late summer.

Dynamics

of populations

549

a

,800

2ooo

220.3

2400

Time

200

100

600

(hrs)

2.0 1.9 1.8 1.7 mE 1.6 ;

1.5

k

1.. ul 1.3

E

l.2 1.1 1.0 as aa L 2000

2100

2200

2300

2400

Time

I

2000

2100

loo

200

300

400

500

(hrs)

2200

2300 2400 . 100 ma 300 400 500 Time (hrs) Figure 2. Fluctuations of ATP, CHL, and tide height during a June spring tide: (a) at the transect, (b) ATP at tall (MF-1) and medium (MF-2) height Spartim within the flume, (c) CHL at tall (MF-1) and medium (MF-2) height Spartina within the flume.

The fluctuation pattern for ATP at the flume was similar to that observed at the transect [Figures 2(b), 3(b)]. The first water parcel entering the tall Spartina contained as much as 50° ,, more ATP than the next parcel of water entering 15 to 30 minutes later.

a

3.2 t 3.0 t

I*

17

Figure 3. Fluctuations of ATP, CHL, and tide height during a September spring tide: (a) at the transect, (b) ATP at tall (MF-1) and medium (MF-2) height Spar&a within the flume, (c) CHL at tall (MF-1) and medium (MF-2) height Spat-rim within the flume.

Dynamics of populations

551

The initial water parcel passingtall Spartina appears to lose a large portion of suspended microbial biomassas a consequence of passagethrough this Spartina zone. The initial sample collected at the medium height Spartim, was taken from water that had already passedthrough tall grass. Levels of microbial biomassin these sampleswere typically 20 to 5oy,o lower in ATP than the initial samplescollected in the tall grass zone [Figures 2(b), 3(b)]. Levels of microbial biomassat both the tall and medium height grassstations fell as tidal height increased, and were typically at minimum levels around high tide. Concentrations increased at both sites astide turned and water left the flume. During flooding tide phases, CHL responded similarly to ATP in that initial levels were high, and fell rapidly as tide height increased. As water progressed from tall to medium height grass CHL levels fell 14 to 60y0. Unlike ATP, CHL levels did not subsequently rise astide began to ebb [Figures 2(c), 3(c)]. Neap tides

During neap tides the tidal signatures of ATP and CHL were essentially the same at both transect and flume. Transect concentrations of both ATP and CHL were typically much lower during flooding tide phasesthan during ebbing tide phases[Figures 4(a), 5(a)]. Occasionally tidal fluctuation patterns were obtained that resembled those typical of spring tides [Figure 5(b)]. In either case, levels of both variables rose rapidly after peak high tide and continued to rise throughout ebbing tide phases. Fluctuations of ATP and CHL at the flume were similar to those obtained at the transect. The initial water parcel entering the flume was low in microbial biomass(either asATP or CHL) compared to levels found during ebbing tides [Figures 4(b), 4(c), 5(c)]. On occasion, dramatic increasesin CHL concentrations occurred during periods of peak ebb discharge [Figure 4(c)].

Discussion Tidally induced fluctuations of ATP and CHL supply insights into the dynamics of microbial populations. Phytoplankton are a component of the biomass measured by ATP analysis and several investigators have reported close correlations between ATP and CHL (Hobbie et al., 1972; Stevenson et al., 1979). It therefore seemsunlikely that the two variables would yield conflicting tidal signatures if the composition of the suspended microbial assemblagedid not change over the course of a tidal cycle. Tidal fluctuation patterns at both the transect and flume suggest that different microbial populations dominate the water column depending upon tide conditions. These data not only confirm information presented by Wilson et al. (1981), but also suggesta possible location within the marsh where the structure of the suspendedmicrobial assemblageis altered. Consider Figures 2(b) and 2(c): both ATP and CHL have essentially the same tidal signatures during flooding phases of the tide. Patterns such as these might be expected if phytoplankton made up a substantial proportion of the total suspended microbial biomassand, therefore, most of the ATP originated with the phytoplankton. Fluctuation patterns differ dramatically during ebb tides, ATP rises while CHL levels remain steady. This pattern indicates that ATE’ extracted from water ebbing from the marsh surface originated with a microbial population other than the phytoplankton. Tidal patterns were different during neap tides. Both total microbial biomass and phytoplankton biomass had similar tidal signatures, low levels of the variables during

552

T. H. Chrzanowski

o.,t*ot I

&J R. Zingmark

tI a6

-

I. 0300

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0700

1100

o*oo

Time

I

b

I

L

OIOO

0700

0800

owe

,000

Time

6,01

,300

(hrs)

0700

osoo

woo

(hrs)

1000

Time (hrs) Figure 4. Fluctuations of ATP, CHL, and tide height during a July neap tide: (a) at the transect, (b) ATP at tall (MF-1) and medium (MF-2) height Spat&a within the flume, (c) CHL at tall (MF-1) and medium (MF-2) height Sparha within the flume.

flooding tides, but elevated levels during ebbing tides. These data suggest that the microbial assemblageis dominated by phytoplankton during both flooding and ebbing phasesof the tide.

Dynamics

of populations

553

Time

(hrs)

Figure 5. Fluctuations of ATP, CHL, and tide height during a August neap tide: (a) ar the transect, (b) ATP at tall height Spartina (MF-1) within the flume, (c) CHL at tall height Spartina (MF-1) within the flume. Insufficient tidal height prevented data collection at the medium height grass.

Tidal signatures of ATP and CHL were similar during flooding spring tides and during neap tides. Consequently, a relatively constant ratio of ATP:CHL would reflect the similarity in patterns. Any consistent increase or decrease in the ratio would reflect a divergence of the tidal signatures. The average ATPCHL ratio was calculated for flooding and ebbing portions of each tidal cycle and the values used to test the hypothesis that the ratio of ATPCHL was greater during ebbing tide phases than during flooding tide

554

T. H. Chrzanowski &R. Zingmark

phases (i.e. the patterns diverge on ebbing tides). The average ratios obtained at the flume were significantly lower on flooding spring tides than on ebbing tides (T-test on arcsin transformed ratios, II= IO tidal cycles, a=O*Ol, tall Spartina and medium Spartina zones treated separately with the same findings). Similar data were obtained at the transect but the critical acceptance level was lower (n= 10, a=0.056). Few data points are available to carry out similar analyses for neap tide conditions (tall Spartina, n = 4; medium Spartina, n = 2; transect, n = 3). However, as might be predicted from the tidal signatures, no significant differences were found between flood and ebb tide ratios for the transect or tall Spartina flume sites. The medium height Spartina site was not separately analysed. Pooling data from the two flume sites increased sample size but did not alter results. The question then arises as to which factors control or regulate separation of microbial populations during tidal action and passage of water over grass flats. Odum et al. (1979) suggested that tidal amplitude (and consequently velocity) may be one of the major factors controlling movements of organic materials through estuarine environments. It seems plausible that a similar model may account for the concentration fluctuation data reported here. During spring tides, velocity of incoming water is sufficient to resuspend material from both the creek bottoms and intertidal zone of Bly Creek basin. The flooding water of oceanic origins pushes the ‘ marsh water ’ remaining in the basin from the previous low tide back into high marsh areas (Stevenson et aZ., 1981). These processes cause the elevated levels of microbial biomass found during early flooding tides. As water elevation continues to rise, the water leaves the creek channels and flows over the grass flats. Falling velocity (due to sheet flow) and dense Spar&a effectively sieve or sediment microflora from the water (but see below). As water exits the grass flats during ebbing tides, organisms (bacteria, fungi, yeasts, possibly protozoans) are resuspended primarily from short and medium Spartina zones (hence the elevated levels of ATP but depressed CHL on outgoing spring tides), and dominate the suspended microbial assemblage. Two lines of evidence support this latter argument. Rublee (1982) has shown that bacterial cells at marsh surfaces have greater biovolumes and biomass than cells contained in waters covering the marsh, and preliminary data from the flume indicate a 20% increase in the number of bacteria during ebbing tide phases. Factors controlling dynamics of the microbial assemblage during neap tides are similar to those during spring tides. Incoming tidal velocities are low compared to those of spring tides and only a portion of the basin intertidal zone is subject to scouring (due to lower tidal amplitude). Consequently, relatively low levels of microbial biomass occur in flooding waters. There is a dramatic increase in biomass levels during outgoing tides and these increases occur early in the ebb at the period of peak water discharge [see CHL, Figure 4(c)], or late in the ebb when the system empties and is subject to convective resuspension [see Figure 5(c) and discussion by Baillie & Welsh (1980)]. During neap tides the tidal signatures of total microbial biomass and phytoplankton biomass are similar. It is apparent from our data that the tall Spar&a zone of the marsh alters the water flowing through/over it and does so to a greater extent during spring tides than during neap tides. During flooding spring tides phytoplankton appear to dominate the suspended microbial assemblage (see opening paragraph of Discussion), but phytoplankton biomass appears to be depressed in ebbing tidal waters [Figures 2(c) and 31. This

Dynamics of populations

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suggeststhat somemechanism is present that favors either grazing of phytoplankton or entrapment of cells in the marsh during spring tides that is not present during neap tides. Our data further suggest that removal of CHL occurs in the tall Spartina zone at the boundary between the tidal creeks and the surface of the marsh [compare tall Spartina concentrations (MF-1) to medium height Spurtinu (MF-2) in Figures 2(b) and 2(c) with 3(b) and 3(c)]. Two mechanisms that may account for these findings are presented below. The first concerns the possible grazing of phytoplankton in the region of tall Spurt&z, and the second concerns production of mucus by various benthic organisms. High densities of grazers in the tall Spurtina region could remove significant amounts of total suspendedmaterial from the water column. Herbivorous zooplankton organisms have been observed to congregate in large concentrations in the top few centimeters of water at the boundary of the creeks and creek banks. These organisms include various calanoid copepods as well as larval stagesof various benthic epifauna (e.g. crustacean nauplii, molluscan veligers, echinoderm plutei, sponge planulae and armelid trochophores). They seemto be most plentiful in the narrow interface between flowing water of the adjacent tidal creeks and the lower velocity water that spills over the top of the marsh (D. Allen, personal communication). Benthic suspension feeders such as the mussel Geukensia demissu, may alsoplay a role in removing material from the water. The second, more intriguing speculation, concerns mucus production by various benthic organisms and the role of these secretions in aggregating suspendedmaterials. Mucilaginous secretions have been shown to stabilize marsh sediments (Holland et al., 1974), to aggregate suspendedmaterial as planktonic diatoms (Ribelin & Collier, 1974) and to contribute to sedimentation and transport processesin tidal Juncus roemurianus marshes(Ribelin 8zCollier, 1974). Diatoms, particularly those pennate diatoms with a raphe, secretea sticky mucilage as a consequence of their benthic movements (Drum & Hopkins 1966; Gordon & Drum, 1970; Harper, 1977). Others secrete mucilaginous threads, pads, stalks tubes or gelatinous capsules(Darley, 1977). Still other speciesform massesor filaments of cells within a common gelatinous matrix (Main & McIntyre, 1974). Raphe-containing diatoms have been reported as the dominant epiphytes on Spartinu ulternifloru in a Louisiana salt marsh (Stowe, 1982) with the highest concentrations occurring on plants in the tall Spurtinu zone. The most active vertical and horizontal movements of estuarine diatoms occurs during daylight hours at low water when cells are exposed by tides (Aleem, 1950; Faure-Fremiet, 1951; Williams, 1962, 1965). Other organisms contribute to the production of sticky mucus on the marsh surface and on Spartina plants. The mud snail Zlyunussu obsoletu hasoften been observed in high densities in the tall Spurtina zone in North Inlet and deposits a slime trail as it crawls across the sediments. Numerous polychates in the Spurtina produce mucus, and the snail Littorina irroratu leaves slime trails on the Spurtinu as it grazes on stem and leaf epiphytes (R. Feller, personal communication). Presumably then, the longer mucus-secreting organisms are exposed during low tides (e.g. during spring tides) the more movements occur which prompt the production of more mucilage, resulting in a stickier surface. This process could increase the capacity for the large surface area of the tall Spurtina zone to effectively remove suspendedmatter from the water column on flood tides and account for our observed tidal fluctuation patterns [Figures 2(c) and 3(c)]. Subsequent grazing of the adherent microalgal flora and of mucus aggregates in the water column by schooling fish (e.g. Fund&us spp., juvenile Mugil spp., and perhaps

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Menidia menidia, which are known to invade the Spartina zones during high tide), invertebrates (e.g. Palaemorietes pugio and various speciesof gammarid amphipods) and Littorina irrorata, which residesprimarily on the Spartina plants, could remove much of the trapped and aggregated flora during the flood tide. Other potential grazers would include various deposit feeders such as the fiddler crab Uca pugilator, which have abundant burrows in the tall Spartina zone, and the meiofauna. Densities of meiofauna are greater in the tall Spartina zone than in the mid or high marsh, and meiofauna are known to emerge from sediments and to concentrate on the mud surface (B. C. Coull, personal communication). In conclusion, there are two salient features of this study: (1) the data indicate that a shift in the composition of suspendedmicrobial assemblagesoccurs during the course of a tide cycle, and (2) the data suggestthat the composition of the suspendedassemblageis altered aswater flows over Spartina dominated grassflats. It is likely that the mechanism accounting for the observed lossof suspendedmicroflora from the water as it passestall Spartina is complex and involves both physical and biological factors. Acknowledgements This work was supported by NSF Grants DEB 8119752 and DEB 8012165. Special thanks Tom Wolaver and to Richard Dame for useful discussionsand to the faculty, technical staff, and students of the Baruch Institute who aided in collection of the field data. References Aleem, A. A. 1950 The diatom community inhabiting the mud-flats at Whitstable. New Phytologist 49, 174-182. Axelrad, D. M., Moore, K. A. &Bender, M. E. 1976 Nitrogen,phosphorus, and carbonflux in the Chesapeake Bay marshes Bulletin 79, Virginia Water Resources Center, Blacksburg, Virginia, USA. 182 pp. Baillie, I’. W. & Welsh, B. L. 1980 The effect of tidal resuspension on the distribution of intertidal epipelic algae in an estuary. Estuarine, Coastal and Shelf Science 10, 165-180. Chrzanowski, T. H., Stevenson, L. H. & Spurrier, J. D. 1982a Transport of microbial biomass through the North Inlet ecosystem. Microbial Ecology 8,139-156. Chrzanowski, T. H., Stevenson, L. H. & Spurrier, J. D. 19826 Seasonal variability and transport of suspended microfungi in a southeastern salt marsh. Applied and Environmental Microbiology 43,392-396. Darley, W. M. 1977 Biochemical composition. In Biology of Diatoms (Werner, D., ed). Blackwell Scientific Publications, Oxford. pp. 198-223. Drum, R. W. &Hopkins, J. T. 1966 Diatom locomotion, an explanation. Protoplasma 62, l-33. Erkenbrecher, C. W. & Stevenson, L. H. 1979 The transport of microbial biomass and suspended material in a high marsh creek. CanadianJournal of Microbiology 24,839-846. Faure-Fremiet, E. 1951 The tidal rhythm of the diatom Hantzschia amphioxys. Biological Bulletin 100, 173-177. Gardner, L. R. & Bohn, M. 1980 Geomorphic and hydraulic evolution of tidal creeks on a subsiding beach ridge plain, North Inlet, S. C. Marine Geology 34,91-97. Glover, L. R. & Morris, I. 1979 Photosynthetic carboxylating enzymes in marine phytoplankton. Limnology Oceanography 23,80-89. Gordon, R. & Drum, R. W. 1970 A capillarity mechanism for diatom gliding locomotion. Proceedings of National Academy of Science USA 67,338-334. Harper, M. 1977 Movements. In BioZogy of Diatoms (Werner, D., ed.). Blackwell Scientific Publications, Oxford. pp. 224-249. Hobbie, J. E., Holm-Hansen, O., Packard, T., Pomeroy, L. R., Sheldon, R. W., Thomas, J. I’. & Wiebe, W. J. 1972 A study of the distribution and activity of microorganisms in ocean water. Limnology and Oceanography 17,544-555. Holland, A. F., Zingmark, R. G. & Dean, J. M. 1974 Quantitative evidence concerning the stabilization of sediments by marine benthic diatoms. Marine Biology 27, 191-196.

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Holm-Hansen, 0. 1973 Determination of total microbial biomass by measurement of adenosine triphosphate. In Estuarine Microbial Ecology (Stevenson, L. H. & Colwell, R. R., eds). University of South Carolina Press, Columbia, South Carolina. pp. 73-89. Holm-Hansen, 0. & Booth, C. R. 1966 The measurement of adenosine 5’-triphosphate in the ocean and its ecological significance. Limnology and Oceanography 11,5 1O-5 19. Kjerfve, B., Stevenson, L. H., Proehl, J. A., Chrzanowski, T. H. & Kitchens, W. 1981 Estimation of material fluxes in an esturine cross-section: A critical analysis of spatial measurement density and errors. Limnology Oceanography 26,325-335. Main, S. I’. & McIntyre, C. E. 1974 The distribution of epiphytic diatoms in Yaquina Estuary, Oregon, USA. Botanica Marina 17,88-99. Nixon, S. W. 1981 Between coastal marshes and coastal waters-a review of twenty years of speculation and research on the role of salt marshes in estuarine productivity and water chemistry, In Estuurine and wetlund processes with emphasis on modeling (Hamilton, R. 81 MacDonald, K. B., eds). Plenum Press, New York. pp. 437-526. Odum, W. E., Fisher, J. S. & Pickral, J. C. 1979 Factors controlling the flux of particulate organic carbon from estuarine wetlands. In Ecological processes in coastal and marine systems (Livingston, R. J., ed.;. Plenum Press, New York. pp. 69-72. Ribelin, B. W. & Collier, A. W. 1974 Ecological considerations of detrital aggregates in the salt marsh. In Ecologicalprocess in coastalmarine systems (Livingston, R. J., ed.). Plenum Press, New York. pp. 47-68. Rublee, I’. A. 1982 Seasonal distribution of bacteria in salt marsh sediments in North Carolina. Estuarine, Coastal and Shelf Science 15,67-74. Stevenson, L. H., Chrzanowski, T. H. & Erkenbrecher, C. W. 1979 The ATP assay, Conceptions and Misconceptions. In Native aquatic bacteria: Enumeration, activity and ecology. American Society for testing and Materials, Philadelphia. pp. 99-l 16. Stevenson, L. H., Chrzanowski, T. H. & Erkenbrecher, C. W. 1981 Temporal fluctuations in the density of filamentous fungal propagules in the water of a high-marsh creek. Mycologiu 73,274-28 1. Stowe, W. C. 1982 Diatoms epiphytic on the emergent grass Spartina alternijoru in a Louisiana salt marsh. Transuctions of the American Microscopical Society 101, 162-173. Williams, R. B. 1962 The ecology of diatom populations in a Georgia salt marsh. Ph.D. Dissertation, Harvard University, Cambridge Massachusetts. pp. 146. Williams, R. B. 1965 Unusual motility of tube-dwelling pennate diatoms.3ournal of l’hycology 1, 145-147. Wilson, C. A., Stevenson, L. H. & Chrzanowski, T. H. 1981 The contribution of bacteria to the total adenosine triphosphate extracted from the microbiota in the water of a salt-marsh creek. Journal of Experimental Marine Biology and Ecology 50, 183-195. Wolaver, T. G., Wetzel, R. L., Zieman, J. C. &Webb, K. L. 1980 Nutrient interactions between salt marsh, mudflats, and estuarine water. In Estuurine Perspectives (Kennedy, V. S., ed.). Academic Press, New York. pp. 123-124.