Hydrobiologia 207: 123-129, 1990.D. J. Bonin & H. L. Golterman (eds), Fluxes Between Trophic Levels and Through the Water-Sediment Interface. 123© 1990 Kluwer Academic Publishers. Printed in Belgium.

Oxygen profiles in intertidal sediments of Ria Formosa (S. Portugal)

Vanda Brotas,l, Ana Amorim-Ferreira, 1 Carlos Vale? Fernando Catarino 1

1Departamento de Biologia Vegetal, Faeuldade de Cieneias de Lisboa, Campo Grande, Bloeo C2, 1700Lisboa, Portugal; 2Instituto Naeional de Investigac;ao des Peseas, A v. Brasilia, 1400 Lisboa, Portugal

Microelectrode oxygen profiles were measured in intertidal sediments from Ria Formosa (S. Portugal),a very productive shallow coastal lagoon. Four intertidal sampling sites were selected according todifferent sediment characteristics. Individual profiles revealed a high degree of lateral variability on acentimeter spatial scale. Nevertheless, consistent differences were observed between oxygen profilesmeasured in atmosphere-exposed and inundated intertidal sediments: in organically poor sand oxygen-penetration depth varied from 3 mm in inundated cores to more than 7 mm in exposed ones, while inorganically rich muddy sand and mud it remained between 0.5-2.0 mm. The oxygen input from inundatedto exposed conditions was estimated for each sampling site. Semi-diurnal tidal fluctuation, leading toperiodical atmospheric exposure of sediments plays a major role in the oxygenation process of intertidalzones of Ria Formosa.

A thin oxygenated layer is commonly observed onthe sediment surface of aquatic ecosystems(Revsbech et al., 1980a; Lindeboom et al., 1984;Baillie, 1986; Andersen & Helder, 1987;Silverberg et al., 1987). At the sediment surface,oxygen is rapidly consumed, either by aerobicdegradation of organic matter and respiration ofbenthic communities, or by reduced compoundsproduced in anaerobic layers and transportedinto the oxygenated zone. The oxygen required byall these reactions can be supplied by the watercolumn, by the atmosphere and may also be pro-duced by photosynthesis within the uppermostsediment layer.

In recent years, membrane-covered polaro-graphic oxygen sensors have been developed to

assay dissolved oxygen gradients near the sedi-ment surface with a sub-millimeter spatial resolu-tion (Revsbech et ai., 1980b; Helder & Bakker,1985). Measurements performed in deep coastalsediments generally show an oxygen penetrationof a few millimeters (Revsbech et al., 1980a;Silverberg et al., 1987). Mechanisms other thandiffusion seem to dominate the oxygen supplyacross the sediment-water interface (Silverberget ai., 1987). In intertidal sediments, however,several sources of oxygen production, oxygenuptake and oxygen transport are present, result-ing in large variations in the oxygen profiles.Several studies have demonstrated that micro-algae photosynthesis increases oxygen concen-tration in the fIrst sediment millimeter (Revsbechet al., 1981, Revsbech & Jorgensen, 1983). Morerecently Baillie (1986), has emphasized the impor-

tant effect of infusion associated with the tidal.fluctuation on the oxygenation of intertidal sedi-ments.

The present study reports oxygen profilesmeasured in intertidal sediments with differentcharacteristics in air-exposed and inundated con-ditions. The results obtained point out the effectof tidal height fluctuations associated with peri-odical atmospheric exposure on the oxygenationprocesses of intertidal areas.

The study area was located in Ria Formosa, ashallow mesotidal coastal .lagoon (mean depth3.5 m), on the south coast of Portugal, perma-nently connected to the sea through several nar-row channels and with no relevant freshwaterinput (Fig. 1). Salinity values average 36 % allyear round. The exposed intertidal area may reach50 km2 (ca. 1/3 of the total lagoon area) at lowwater during spring tides and almost 20 % of thisarea is occupied by growth-banks of the clam

Ruditapes decussatus L.. Large areas of the lagoonare covered by macrophytes (Zostera spp andmacro algae). To evaluate the spatial variability ofsediment oxygenation in the intertidal zone, foursites were selected (Fig. 1): station 1 a sandy clamgrowth bank, station 2 a muddy sand clamgrowth bank, stations 3 and 4 both located onmudflats not used for aquaculture, but station 4had a higher carbon content. These sites emergefor about two hours during spring tides. At sam-pling time (always between 10 and 12 a.m.) sedi-ment temperature ranged from 17 °C in winter to28°C in summer.

From January 1988 to February 1989, sedi-ment samples were collected three times duringthe winter period and once every month in thesummer period. All samples were drawn while thesediment was atmosphere-exposed at low tide. InJanuary 1990 both atmosphere-exposed and in-undated sediments were collected at the samesites, at low and high tide. Samples were taken byhand with plexiglass tubes (15-20 cm length and8 cm i.d.) which were immediately stoppered atthe bottom with an hermetic lid and brought to the

ATLANTIC

OCEAN

laboratory. Inundated cores were transported ina basin containing water from the samplinglocality several centimeters in depth. In January1988, sediments from stations 1 and 2 were col-lected undisturbed and put inside transparentplexiglass box cores (40 x 40 x 30 cm). Thesewere subsequently covered with water from thesampling locality (ca. 20 cm depth) and trans-ported to the field laboratory where they were keptoutdoors for two weeks under shade, with con-tinuous stirring and aeration to maintain oxygenin the overlying water at saturation levels.

For each sampling station sediment was ana-lyzed for grain size, organic carbon, chlorophyll a,phaeopigments and water content. The sandfraction was determined by sieving and the otherfractions by means of a sedimentometer. Organiccarbon were estimated by subtracting the in-organic carbon from total carbon content meas-ured separately in a CHN-analyzer. Concentra-tions of chlorophyll a and phaeopigments in theupper centimeter were determined spectrophoto-metrically according to Lorenzen (1967). Watercontent was calculated by weighing the sedimentsbefore and after drying to constant weight at105 0 C. Porosity was expressed as the ratio ofwater volume to water volume plus volume ofsediment sample.

The vertical distribution of oxygen was studiedin the laboratory at room temperature (20- 24 0 C)and room light intensity (10 p.E m - 2 S - I ), with apolarographic needle sensor (2.5 cm length,0:7 mm o.d.). Oxygen needle electrodes are indi-cated for coarse-grained sediments providing agood spatial resolution (0.25 mm), (Helder &Bakker, 1985). In situ measurements wereattempted without success. The pore water move-ments created by the operator standing on themud- and sand-flats made it impossible to makevaluable measurements. The needle electrode(produt n° 760), the chemical microsensor(n 0 1201) and Agj AgCl reference electrode(n 0 334) used in this study, were purchased fromDiamond Electro-Tech Inc., Ann Arbour,

ichigan, USA.Before each experiment the electrode was

allowed to stabilize at - 0.7 Vat the measurement

temperature in filtered water from the lagoon forat least 2 hours. The electrode was calibrated inoxygen saturated water from the lagoon (21 % O2)

and in deep anoxic sediment (0 % O2), The refer-ence electrode was always introduced in thecalibration media as well as the measurementmedia (sediment or water). Stabilization wasalways confirmed with a strip chart recorder.When measuring the oxygen profiles the needleelectrode was lowered into the sediment at0.25 mm intervals using a manual micro-manipulator. In inundated cores the overlyingwater above the sediment was 1-2 cm deep.

The oxygen profiles were measured on fieldsamples in two situations: (i) undisturbed sedi-ment cores one hour after collection (both atmos-phere-exposed and inundated); (ii) atmosphereexposed sediment cores, which were subsequentlyimmersed with water (oxygen saturated) from thesampling locality and allowed to stand with nostirring for 10 hours. Measurements were alsoperformed in sediments collected from the boxcores previously described, 14 days after fieldsampling.

Oxygen concentration was measured in coarse-and fine-grained sediments containing low- andhigh-organic matter. Sediment characteristicswithin the upper 5 cm of the cores collected at thefour sampling sites are presented in Table 1.

In order to evaluate the effect of time lagbetween collection and measurement of oxygenprofiles in air-exposed cores, sequential profileswere measured in the laboratory at 10, 30, 60and 120 minutes after collection (Fig. 2). Duringthe first 60 minutes slight differences wererecorded in the oxygen penetration depth whichmay be attributed to small-scale spatial hetero-geneity. However, after this period, penetrationdepth decreased and surface value increased,defining a different oxygen profile. Therefore, weassume that only measurements within one hourwere reliable.

Profiles of dissolved oxygen measured in air-

Table 1. Sediment characteristics of the sampled cores within the upper 5 em; chlorophyll a and phaeopigment content representannual average values of the upper sediment centimeter; water content was determined for inundated and air exposed sediments,there were no significant differences between these two conditions.

~~(t~St2 St 3 St4

~~0

Sand 0 > 60 Ilm (%) 97.3 81.2 23.2 14.0Silt 211m < 0 < 60 Ilm (%) 2.4 16.0 67.3 76.6Clay 0 < 21lm (/0) 0.2 2.8 9.5 9.4Water content 0.18 0.36 0.49 0.61Porosity 0.34 0.56 0.72 0.80Organic carbon (%) 0.20 1.46 1.68 2.80Chlorophyll a I1gg- I dw 4.39 7.42 6.19 2.96Phaeopigments J1gg- I dw 4.42 13.77 18.86 12.69

exposed sediments from stations 1 to 4, at twodifferent sampling periods, are presented inFig. 3. In spite of variations in the same core andbetween sampling periods, there were consistentdifferences between the stations in both the oxy-gen penetration depth and in the shape of theprofiles. Oxygen penetrated down to 0.5-1.0 mmin mud (stations 3 and 4), to 1.0-1.8 mm inmuddy sand (station 2) and to 6 mm or more insand (station 1). Oxygen variation with depth wasquite irregular at station 1, while exponential toalmost linear distributions were found for theother stations. The oxygen gradients at stations 2,3 and 4 varied from 105 to 395 jiM mm - 1 whileat station 1 they were always lower than 90 jiM

mm-I.Oxygen profiles were also measured in cores

collected from the atmosphere-exposed andinundated intertidal areas of the same stations

0 ..0

0,5

E 1.0E1.5

.c:Q.

2.0Q)

02.5

3.0a 100 200

11M 02

Fig. 2. Study of time-lag effect. Oxygen profiles in anexposed and muddy sand area (March 1988): 10 min (+ ),

30 min (*), 60 min (D) and 120 min (x).

(Fig. 4). At stations 2, 3 and 4, oxygen penetra-tion depths in exposed and inundated sedimentswere quite similar. A different picture was foundat station 1: the erratic variation with depthobserved in most exposed cores was not found in

.c:Q.g 0,0

Fig. 3. Vertical oxygen profiles measured in air-exposedsediment cores at two different sampling periods (solid anddashed lines). Two replicate profiles are presented for eachperiod. In spite of seasonal and small-scale spatial variations,consistent differences between cores in both depth penetra-

tion and shape of the profiles are evident.

0.0 0.0

0.52.0

1.04.0

1.5 StatIon 26.0 Station 1

E 2.0

E 0 100 200 0 100 200

.c0.

oo~Q)

I0.0

Cl

0.50.5

1.0 1.0

1.5 1.5Station 3 Station 4

2.0 2.0

0 100 200 0 100 200

UM 02

Fig. 4. Oxygen profiles in air-exposed (solid line) andinundated (dotted line) sediments collected in January 1990at low and high tide, respectively. In the inundated coresoxygen concentration in the bulk of the overlying water was180 JlM for stations I and 2, 138 JlM for station 3 and170 JlM for station 4. Oxygen saturation value at measuring

temperature was 234 JlM.

inundated conditions and penetration depth de-creased substantially. At stations 2, 3 and 4 sur-face levels of oxygen in air-exposed sedimentswere higher than in inundated ones. For all sam-pling stations, oxygen gradients were 2-3 foldsteeper in exposed cores than in inundated ones:13 versus 55 f.LM mm - I at station 1, 125 versus220 f.LM mm - I at station 2, 50 versus 180 f.LMmm - I at station 3, 130 versus 230 f.LM mm - I atstation 4.

According to the Fick's law of diffusion,J = 0 Ds !J.Cj!J.x, the oxygen flux (J) at each core(for constant values of porosity, 0, and sedimentdiffusion coefficient, Ds) increases as thegradient,!J.Cj!J.x is higher. This means that oxygenfluxes across the sediment-water interface arehigher in the exposed cores than in the inundatedones.

The amount of oxygen (Q) present in the sedi-ment, from the sediment-water interface (pO) tothe maximum depth of oxygen penetration (pmax)may be calculated by unit area as follows:

Q = w J C(p) dp[pO, pmax]

where w is the water content and C the oxygenconcentration at the oxygen penetration depth, p.

Based on oxygen profiles (Fig. 4) and watercontent measurements (Table 1), one may calcu-late the amount of oxygen at exposed (Qe) andinundated cores (Qi) of each site.

Assuming that oxygen profiles obtained arerepresentative of the conditions encountered inthese locations, the difference Qe - Qi, at eachstation, represents the oxygen input from in-undated to exposed periods. The result ofQe - Qi was positive for all the stations: from 16to 2 nmol cm - 2 at station 1, 0.8 nmol cm - 2 atstation 2, 2.7 nmol cm - 2 at station 3, and1.5 nmol cm - 2 at station 4. Except for station 1,where the irregularity of replicate profilesaccounted for a large range of Qe - Qi, the othersites presented a comparable oxygen input.

Oxygen profiles measured in sediment coresfrom stations 1 and 2 artificially immersed in thelaboratory for 10 hours are presented in Fig. 5. Adiffusive boundary layer above the sediment sur-face was formed. Jorgensen & Revsbech (1985)relate the thickness of this layer to the rate of

~ -4

E

-=- -2.c0. aQ)Cl

UM 02

Fig. 5. Oxygen profiles measured in sediment cores fromstation 1 (+) and station 2 (x) artificially immersed in thelaboratory for 10 hours. Oxygen saturation value at measur-

ing temperature was 206 JlM.

oxygen uptake of sediment surface: when steepgradients are established, the boundary layer mayrepresent a major resistance to the transport ofoxygen; whereas in sediments with a low respira-tion rate, diffusion through this layer does notplaya significant role for oxygen uptake. Figure 5indicates a higher rate of oxygen uptake for sedi-ment of station 2, as the thickness of the diffusiveboundary layer was 3 mm compared to 0.5 mm inthe sediment from station 1. Furthermore, thesediment oxygenated layer recorded at station 2was thinner (1.3 mm) than at station 1 (1.8 mm).In comparison with inundated cores (Fig. 4), thepenetration depth was particularly reduced atstation 1. This represents a reduction of oxygenflux from 20 nmol cm - 2 h - 1 in __exposed to13 nmol cm - 2 h - 1 in inundated sediments(Ds = 2 x 1O-scm2s-1,for20 °C, Andersen &Helder, 1987).

Oxygen measurements in 14-day incubatedsediments from stations 1 and 2, revealed almostlinear profiles, oxygen dropping to 2.0-2.8 mm(Fig. 6). With stirring and continuous air-supply,oxygen penetration in sediment from station 1 iscomparable to that recorded in inundated condi-tions, but in sediments from station 2, oxygenwent 1.5 mm deeper (compare Figs. 4 and 6).Similarly, the comparison between 14-day andlO-hour incubations shows that at station 2 oxy-gen went 1 mm deeper, as oxygen is supplied tothe overlying water, whereas at station 1 penetra-tion depth remained roughly the same. The highercarbon content in sediments from station 2accounts for the oxygenation differences between

200 0IJM 02

Fig. 6. Oxygen profiles measured in cores collected fromsediment incubated with continuous stirring and aeration for

14 days. Three replicates are indicated for each core.

the experiments; Lindeboom et al. (1984) drewthe same conclusion, from sediments with lowand high POC content, in a shallow brackish lake.

Oxygen fluxes into the sediment were 35 and59 nmol cm - 2 S - 1 for stations 1 and 2, respec-tively, in the 14-day experiment; whereas in thelO-hour experiment they were 22 nmol em - 2 S - 1

for station 1 and 34 nmol O2 em - 2 S - 1 forstation 2 (see Figs. 5 and 6). Oxygen fluxes calcu-lated in this study are comparable to thosereported for shallow nearshore marine sediments(Silverberg et al., 1987; Andersen & Helder,1987).

The results obtained in this study point out thecontrasting oxygenation of sand/mud-exposed/inundated intertidal surface sediments of RiaFormosa. While in mud and muddy sand theoxygenated layer was thin (0.5-2.0 mm) under allthe experimental conditions, a deeper and var-iable layer was found in sandflats (from 3 to morethan 7 mm).

Exposure of sand to the atmosphere seems tobe the major cause for the high oxygen pene-tration. The irregularities found in most oxygenprofiles in sand, may be due to the presence of airbubbles which favor the diffusional exc,hange of

. oxygen with the deeper interstitial water retainedaround particle grains (Revsbech & Jorgensen,1983). Revsbech etal.,(1981) demonstrated thatoxygen levels in surface sediment may increasedue to micro algal photosynthesis. In ourmeasurements, autochthonous production ofoxygen in exposed sand cannot alone justify mud-sand oxygen penetration differences. In fact,values of chlorophyll a were comparable in all thesampling locations and experiments were per-formed under similar light conditions.

Reduction in the thickness of the oxygenatedlayer in inundated sand probably results from theinterruption of atmospheric oxygen supply tosand interstices with the rise of water level. Riedl& Machan (1972) studied the dynamics of inter-stitial water in intertidal sand and demonstrated

the existence of a filling-draining process drivenby the tidal height fluctuation. This pulsingmechanism may lead to the transport of oxygenfrom the atmosphere as well as the transport ofreduced substances from deeper anaerobic layers(Fenchel, 1978). In mud, this pulsing mechanismtends to be less effective. Penetration depth wascomparable in inundated and exposed conditions,but oxygen increased considerably in the surfaceof exposed mud.

The discrepancy of oxygen profiles at stations 1and 2, both with a high percentage of sand (97 %and 81 %, respectively), may be related to thedifferent organic matter content. Anderson &Helder (1987) showed that large differences inoxygen depth penetration may be due to bothorganic matter content and wave exposure. In-filtration of water between sand grains results ina faster turnover rate of easily degradable organiccarbon at the exposed sites. In our study, station1 is situated near the inlet channel of the lagoon,whereas station 2 is located in an inner area (seeFig. 1). Consequently sediments of station 2 havea minor wave exposure, which may result in apoorer renewal of interstitial water. This leads toa progressive accumulation of organic matter inthe sediments.

The differences in oxygen penetration in sedi-ments from stations 1 and 2 were drasticallyreduced in the 14-day incubation experiment.When tide-driven renewal of interstitial water isabsent, the oxygenation of the sediment surfacedue to diffusional processes and net production ofoxygen, is similar in both sediments.

Baillie (1986) pointed out the role of the tideand micro algae photosynthesis in the oxygenationprocess of sediment surface of intertidal areas.The experiments conducted in this study havesimply emphasized the question of how the oxy-genated layer varies from exposed to inundatedconditions in sediments of Ria Formosa. Studiesfrom intertidal (Riedl & Machan, 1972; Baillie,1986) to coastal sediments (Silverberg et ai.,1987) concluded that mechanisms other thanmolecular diffusion must dominate the transportof oxygen across the sediment-water interface. Inour study, the largest differences were observed in

organically poor sands between atmosphere-exposed and inundated periods. These are mainlyattributed to transport processes through porewater movement, which are driven by the largefluctuation of tidal height. Evapotransport,coupled with respiration, deplecting the oxygen inorganically rich sediments, accounts for the thinoxygenated layer. These processes may be par-ticularly intense in summer due to the high tem-peratures of the water lagoon. However, seasonalchanges were not observed, probably because ofthe small-scale temporal variations of the oxy-genation process. Further studies should there-fore be conducted to understand the role ofbottom primary producers coupled with the semi-diurnal effect of tide on the formation andmaintenance of the oxygenated surface layer onthe sediments of intertidal zones.

We thank M. Falcao for all help and facilitiesprovided during this study, and Prof. S. Prates forthe granulometry analysis. This work was sup-ported by the Portuguese Junta Nacional de In-vestiga<;ao Cientifica e Tecnol6gica (JNICT) bycontract n° 869.86.141.

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