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Gebersdorf et al 05
AQUATIC MICROBIAL ECOLOGY
Vol. 41: 181–198, 2005 Published November 25
Aquat Microb Ecol
Microphytobenthic primary production in the
Bodden estuaries, southern Baltic Sea, at two
study sites differing in trophic status
Sabine Ulrike Gerbersdorf 1, 2,*, Jürgen Meyercordt 1, Lutz-Arend Meyer-Reil1
1
Institut für Ökologie, Ernst-Moritz-Arndt-Universität Greifswald, Schwedenhagen 6, 18565 Kloster/Hiddensee, Germany
2
Present address: Institut für Wasserbau, Versuchsanstalt, Pfaffenwaldring 61, Universität Stuttgart, 70550 Stuttgart, Germany
ABSTRACT: Eutrophication in coastal areas has stimulated phytoplankton growth, sustaining a high
biomass and leading to a shift in the underwater light field. With the significance of the microphyto-
benthos for oxygen supply and carbon budget of both benthic and pelagic habitats in mind, the pos-
sible effects of reduced light availability were investigated in the estuarine Bodden area (southern
Baltic Sea) at 2 sites differing in trophic status — the eutrophic Kirr Bucht (KB) and the mesotrophic
Rassower Strom (RS). Using for the first time microsensors in Bodden sediments, it was possible to
visualize small-scale heterogeneity in the light regime, photosynthetic activity and oxygen penetration
with high spatial and temporal resolution. Hence, differences at the 2 sites related to sediment charac-
teristics (KB sandy, RS muddy), and photoautotrophic biomass (benthic chlorophyll a in the upper
1 cm, µg cm– 3 = 11 to 48 at KB and 13 to 17 at RS) could be ruled out. Calculations of benthic primary
production based solely on microelectrode measurements revealed substantial oxygen fluxes and car-
bon fixation rates at in situ light intensities at both study sites (e.g. gross primary production, GPP, mg
C m–2 h–1 = 28 to 80 at KB and 3 to 36 at RS). The different combinations of water transparency (pelagic
chlorophyll a, µg l–1 = 12 to 33 at KB and 1.3 to 4.5 at RS), light attenuation k (3.17 m–1 at KB, 0.61 m–1
at RS) and water depth (0.6 m at KB, 3.4 m at RA) have led to a similar light availability for benthic
algae on the sediment surface at both study sites. Consequently, the benthic algae had comparable
productivity at both sites, with maximum primary production, P Bmax (mg C mg–1 chlorophyll a h–1) of
0.29 to 1.46 at KB and 0.17 to 1.63 at RS; and were adapted to rather low light conditions, with light
saturation, Ek (µE m–2 s–1) of 22 to 152 at KB and 10 to 116 at RS). Varying with season, microphytoben-
thic photosynthetic activity accounted for 26 to 59 and 2 to 53% to the total primary production at the
KB and RS, respectively, with the highest contribution in spring coincident with the most favourable
light conditions at the sediment surface. With an annual average of about 37 and 30% (KB and RS, re-
spectively), the contribution of the microphytobenthos to total production was significant and compa-
rable at both study sites. Nevertheless, the higher trophic status at KB resulted in a change in the ben-
thic microalgal community towards sedimentated phytoplankton species and had a negative impact
on microphytobenthic primary production rates. This was estimated by calculating the gross primary
production for varying water depths on the basis of the different water transparency at the 2 sites.
KEY WORDS: Microphytobenthos · Primary production · Microsensors · Microprofiles · Phytoplankton ·
Benthic–pelagic coupling · Estuary · Baltic Sea
Resale or republication not permitted without written consent of the publisher
INTRODUCTION phytobenthos is presumed to be important in stabilis-
ing sediments (de Brouwer et al. 2003) and in con-
In shallow non-tidal waters, the light climate allows trolling nutrient fluxes directly at the sediment/water
the development of a photoautotrophic benthic com- interface through nutrient uptake (Sundbäck et al.
munity (Wasmund 1986, Miller et al. 1996). The micro- 1991, Rizzo et al. 1992, Wiltshire 1992). Moreover,
*Email: sabine.gerbersdorf@iws.uni-stuttgart.de © Inter-Research 2005 · www.int-res.com
182 Aquat Microb Ecol 41: 181–198, 2005
oxygenation of the sediment surface layers by photo- tat and its role as an important link in benthic–pelagic
synthetic activity leads to indirect geochemical fixation coupling after resuspension events (Gerbersdorf et al.
of nutrients and heavy metals (Koop et al. 1990, 2004).
Nielsen et al. 1990). Furthermore, the supply of oxygen Herein, we report the first comprehensive investiga-
through photosynthetic activity determines the occur- tions on microphytobenthos over a seasonal range to
rence of heterotrophic organisms such as protozoans be carried out in the Bodden estuaries at 2 study sites
and meiofauna in the upper sediment (Berninger & differing in trophic status. In contrast to recent pub-
Epstein 1995). In terms of primary production, the lications (Meyercordt & Meyer-Reil 1999, Meyercordt
microphytobenthic community may account for the et al. 1999), microphytobenthic primary production
main part of carbon fixation, especially in shallow rates in the present study were determined solely by
waters (Cadee & Hegeman 1974, Plante-Cuny & Bodoy microelectrodes. Moreover, interpolation of the data
1987, MacIntyre & Cullen 1996, MacIntyre et al. 1996, for the time intervals between measurements was
Underwood et al. 2004). done using the Walsby (1997) model. Especially in the
During the last few decades, phytoplankton growth low light range, microelectrode measurements are far
has been stimulated in many coastal zones by an in- more sensitive than other integrative methods, and
creased supply of nutrients, which sustains a high bio- allow the direct determination of gross photosynthesis
mass and has led to a shift in the underwater light rates within the sediment (Revsbech et al. 1981, Revs-
climate (Radach et al. 1990, Schiewer 1998). Several bech & Jørgensen 1983, Sommer 1994, Karsten & Kühl
publications have dealt with the pelagic primary pro- 1996, Gerbersdorf 2000). Thus, the measurements of
duction in the Bodden estuaries (estuarine areas in benthic production rates are more reliable, and hence
the Southern Baltic Sea, hereafter referred to as ‘the calculations on the sediment oxygen budget and car-
Bodden’) (Hübel 1968, Börner & Kell 1982). These pub- bon supply to the benthic habitat as well as to the
lications have clearly documented increased phyto- pelagic habitat after resuspension are more precise.
plankton biomass and primary production rates related Moreover, microprofiles of light and oxygen reveal
to change in the trophic status over the last 30 yr mutual changes in abiotic factors and the resulting
(Wasmund 1990, Wasmund & Schiewer 1994, Bachor microphytobenthic photosynthetic activity at high spa-
et al. 1996, Hübel et al. 1998). Increased phytoplankton tial and temporal resolution, which can only be
abundance has led to a reduction in light penetration detected as a sum otherwise (Revsbech & Jørgensen
and hence a decline in macrophytes and submerged 1986, Lassen et al. 1992). The Walsby (1997) model
flowering plants (Behrens 1982, Teubner 1989). The takes the reflection characteristics of the light at the
change in the underwater light climate may also signif- water surface under different solar angles into consid-
icantly affect the microphytobenthic primary produc- eration. Hence the calculations of the underwater light
tion, as light intensity is considered to be the primary field and corresponding production rates (especially
factor controlling benthic photosynthesis (Colijn 1982, with regard to the different trophic status of the 2 study
Pickney & Zingmark 1993). Despite the significance of sites) achieved further precision in the present study.
the microphytobenthos, comparatively little data has Possible physiological adaptations of the benthic algae
been published on microphytobenthic primary produc- to prevailing light conditions were examined using
tion and the possible effects of eutrophication, globally photosynthesis/irradiance (P /E) curves with data on
and for the sublittoral in particular. For the Bodden, maximum photosynthetic capacity (Pmax), photosyn-
only a few studies have focused on the microphyto- thetic efficiency (α) and the light saturation coefficent
benthic community and primary production rates (Ek) (Kohl & Nicklisch 1988, Pickney & Zingmark 1991,
(Täuscher 1976, Krause 1977, Wasmund 1986). To Falkowski & Raven 1997, Barranguet et al. 1998).
date, almost nothing has been recorded on the present To examine possible effects of eutrophication on the
status of microphytobenthos in the Bodden in general benthic microalgal community (Sundbäck & Snoeijs
and the possible effects of light limitation on microphy- 1991), the species composition of the phytoplankton
tobenthic production and community dynamics in par- and microphytobenthos was determined microscopi-
ticular. Only recently has data on the primary produc- cally at the 2 study sites.
tion rates of benthic microalgae and their contribution
to the total primary production of the shallow Bodden
as a function of trophic status been reported (Gerbers- MATERIALS AND METHODS
dorf & Meyercordt 1999, Gerbersdorf et al. 2000). The
photoautotrophic character of the flocculent sediment Study sites. Two study sites in the estuarine Bodden
surface layer, its fractions and its aggregates indicated area, southern Baltic Sea (Fig. 1) differing in morpho-
the significance of the microphytobenthos in the Bod- metry, hydrography and trophic status, were investi-
den for the oxygen/carbon budget of the benthic habi- gated at different seasons. The Kirr-Bucht (KB) is an
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 183
Sampling and treatment. Sampling took
place once each season (July 1996, Sep-
tember/October 1996, January 1997, April
1997) at each study site. For benthic pri-
mary production measurements, undis-
turbed sediment cores of about 100 mm
length and 1.1 l of overlying ambient water
were taken using cylindrical Plexiglas
tubes (length 300 mm, internal diameter
100 mm) either with a hand-manipulated
coring device or with a multicorer device
(Barnett et al. 1984) at Sites KB and RS,
respectively (the device used depended
on the shallowness of the investigation
area). The sediment cores were carefully
transported to the laboratory and placed in
a room protected from electrical ‘noise’.
Sediment cores were placed into a water
bath and the in situ temperature was
kept constant by a cooling system. During
photosynthesis measurements, the sedi-
ment cores were illuminated under differ-
Fig. 1. Study sites. A: Kirr Bucht (inner part of the Darss-Zingster Boddenkette);
B: Rassower Strom (outer part of the Nordrügensche Boddenkette), both located ent light intensities by a halogen cold light
in the estuarine Bodden area of the southern Baltic Sea. DK: Denmark source (Schott, KL 1500 electronic), with
the lamp at a 45° angle to avoid shading
by the microsensor. The exposure of the
inner area in the Darss-Zingster Boddenkette, charac- samples to different irradiances (ranging from in situ to
terised by low salinities (5.0 to 6.6) and high nutrient artificial high light intensities) was alternated by dark
concentrations (Gerbersdorf et al. 2004, S. Dahlke pers. periods. The water column above the sediment was
comm.). Its high chlorophyll a concentrations (12 to aerated to keep the oxygen concentration constant. To
33 µg l–1) and pelagic primary production rates (Hübel measure pelagic primary production and respiration,
et al. 1998) are typical for eutrophic waters (Wasmund water samples were incubated in situ in 3 sets of 4
& Kell 1991). In a water depth of 0.6 m, the sediment is transparent and 4 black bottles over a period of about
sandy with an organic carbon content of 1%. Rassower 10 h. Each set of bottles was exposed at a different
Strom (RS) is one of the outer Bodden estuaries of the water depth (below surface, above bottom and mid
Nord-Rügensche Boddenkette, and consequently is water; for further details see Meyercordt et al. 1999).
more strongly influenced by the Baltic Sea, having Natural light intensities at sediment surface. Nat-
higher salinities (8.2 to 9.4) and low nutrient concentra- ural in situ light intensities experienced by the micro-
tions (Gerbersdorf et al. 2004, S. Dahlke pers. comm.). phytobenthos were calculated for each season for both
Because of its lower chlorophyll a concentrations (1.3 to sites (Table 1). The light attenuation coefficient (k) in
4.5 µg l–1) and pelagic primary production rates (Hübel the water column was calculated from vertical light
et al. 1998), this study site is regarded as mesotrophic intensity profiles in decimetre to metre steps by a
(Wasmund & Kell 1991). The sediment in approxi- spherical underwater sensor (LI-COR LI 193SA). In
mately 4 m water depth consists of sandy mud with an combination with data on photosynthetically active
organic carbon content of up to 4% on its surface. In radiation (PAR, 400 to 700 nm), which was continu-
January 1997, the RS was not accessible due to ice ously measured above the water surface (LI-COR LI
cover. Therefore, another nearby sampling station, the 190SA), k values were used to calculate the lowest,
Klosterloch, which is comparable to the RS in terms of medium and highest irradiances at the sediment
water and sediment characteristics, was used for this surface for the relevant periods (Table 1).
month. (For simplicity, the term ‘Rassower Strom, RS’, Chlorophyll a and phaeopigment a. Pigments in
will be used hereafter for data from Klosterloch and water samples of a defined volume were concentrated
RS.) More details on the morphology and hydrography on Whatman GF/C filters, which were immediately
of KB and RS are available in Correns & Jäger (1979, deep-frozen. The sediment cores were sectioned into
1982), Schlungbaum et al. (1994), Meyercordt et al. different layers at intervals of 1 cm and each layer was
(1999) and Gerbersdorf et al. (2004). mixed thoroughly to avoid patchiness in the pigment
184 Aquat Microb Ecol 41: 181–198, 2005
Table 1. Light attenuation k (m–1) in the water column and and the light sensors were modified after Lassen et al.
range of in situ light intensities (lowest to highest) available to (1992). The precise position of the microsensors was ob-
the microphytobenthos at the sediment surface in the Kirr
served through a dissection microscope, using a micro-
Bucht and Rassower Strom (Bodden area of the southern
Baltic Sea). Irradiance calculated on an hourly basis from manipulator with a control unit (Märzhäuser & Wetz-
constantly measured photosynthetically active radiation lar, Type DC 3-K right and MS314) for positioning.
above the water surface and light attenuation in the water The microsensors determine oxygen gradients at
column, averaged for relevant month the sediment/water interface, caused by photosyn-
thetic and heterotrophic activity, under dark and light
Month k Light intensity (µE m–2 s–1)
conditions. The resulting oxygen fluxes (upwards out
Low Medium High
of the sediment into the water column and downwards
Kirr Bucht into deeper sediment horizons) have been used to cal-
July 1996 3.48 75 180 300 culate oxygen consumption/production (Revsbech et
October 1996 3.31 26 153 222
January 1997 2.17 10 141 197 al. 1981, Sommer 1994). For these calculations, the dif-
April 1997 3.73 18 198 168 fusion coefficient of oxygen in the water and sediments
Rassower Strom as well as the porosity of the sediment must be taken
July 1996 0.57 45 117 180 into account (Li & Gregory 1974, Ullmann & Aller 1982,
October 1996 0.73 12 180 120
January 1997 0.56 20 135 100 Revsbech & Jørgensen 1986, Rasmussen & Jørgensen
April 1997 0.59 19 107 177 1992). Oxygen microelectrodes can also be used to
directly determine gross photosynthesis by the light/
dark shift method (Revsbech et al. 1981, Revsbech &
concentrations. From each sediment layer, 5 subsam- Jørgensen 1983, 1986). Thereby a steady state of
ples of 0.5 cm3 each were taken with a cut-off syringe oxygen distribution will be achieved under constant
and stored deep frozen in centrifuge tubes. Pigment conditions and the initial decrease in oxygen within
analysis following the guidelines of the Helsinki Com- 1 s after darkening the sediment reflects gross photo-
mission (HELCOM 1988). Pigments were extracted in synthesis (Revsbech & Jørgensen 1983, Karsten & Kühl
96% ethanol followed by spectrophotometric readings 1996). This is the only method that takes into account
at 665 nm before and after acidification with HCl to variation in oxygen consumption in darkness and at
correct for the phaeopigment a concentrations (Perkin- different irradiances arising from differential expan-
Elmer UV/VIS spectrometer lambda 2). sion of the oxic layer and/or changes in volumetric
Light and oxygen fluxes. On the assumption that respiration rates in response to oxygen supply (Epping
oxygenic photosynthesis is the main pathway of car- 1996). To avoid changes in oxygen concentration due
bon dioxide fixation in the Bodden, changes in oxygen to osmotic effects, the vertical spatial resolution of the
concentrations were recorded in the water samples light/dark shift method is restricted to layers of approx-
and sediment to calculate pelagic and benthic photo- imately 100 µm by the oxygen diffusion velocity, which
synthesis, respectively. The terms photosynthesis and is 67 µm s–1 according to the Einstein-Smoluchowski
primary production are interchangeable in the law (Neudörfer & Meyer-Reil 1998).
following text. Microscale variations in the occurrence of benthic
Oxygen exchange: Since oxygen fluxes can be organisms and their metabolic activities are well docu-
derived from microelectrode profiles only in sedi- mented (Revsbech et al. 1983, Jørgensen & Revsbech
ments, the pelagic primary production and respiration 1985, review by Meyer-Reil 1994) and may hamper the
was measured in situ by changes in the oxygen con- extrapolation of rates measured by microelectrodes.
centration in water samples under light and dark con- Therefore, to obtain a representative overview of res-
ditions, determined by the Winkler method. The light piration and photosynthetic activity in the sediments, 6
conditions for the incubated water samples were to 12 vertical profiles were taken randomly from the
recorded via a spherical underwater sensor (LI-COR LI sediment surface of each sediment core.
193SA; for further details see Meyercordt et al. 1999.) Primary production. Pelagic gross photosynthesis
Microelectrode measurements: Microsensors were was calculated as the sum of respiration and net photo-
used to determine the light intensity, light attenuation synthesis. Microphytobenthic photosynthetic activity
and the photic zone (zPAR), as well as the oxygen con- was determined similarly, but also directly by the
centration and penetration depth (zoxygen) in the upper light/dark shift method, whereby the gross photosyn-
sediment layers in relation to illumination at the sedi- thesis rates for the different sediment layers were
ment surface. The microsensors enabled measurements related to volume and multiplied by the vertical expan-
of high vertical (50 to 100 µm) and temporal (< 0.1 s) sion (zphot) of the measured profile of photosynthetic
resolution. The Clark-type oxygen microelectrodes activity (Revsbech et al. 1981, Revsbech & Jørgensen
were built according to Revsbech & Jørgensen (1986) 1983, 1986).
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 185
Gross primary production rates were expressed as body, but also the reflection characteristics of the water
C-equivalents using the conversion factor 1.2 (Mills surface. Therefore, calculations of light availability for
& Wilkinson 1986) and taking main substrates and phytoplankton in different water depths as well as for
products of dioxide fixation into account (Burris 1981, microphytobenthos at the sediment surface gained fur-
Raine 1983, Sakshaug et al. 1997). Gross primary pro- ther precision. Using these light field calculations,
duction rates of pelagic and microphytobenthic area pelagic primary production was calculated in 0.1 m
were normalised to chlorophyll a concentrations in the steps from the water surface down to the bottom, and
water samples and in the flocculent sediment surface integrated over the whole water column on an hourly
layer, respectively, to correct for algal biomass. The basis. Benthic primary production and respiration
different resolution of sediment pigment profiles were also calculated on an hourly basis using the
(0.5 cm steps in the upper layers) and oxygen/gross calculated PAR values at the sediment surface.
photosynthesis microprofiles (100 µm) did not allow Statistics. The assumptions of normality and homo-
appropriate algal biomass correction, and represents a geneity of variance were tested using visual assess-
challenge for further experiments. ment of the frequency histogram and normal plot, as
Photosynthesis models. In a literature overview, well as skewness and kurtosis, both of which provide
Jassby & Platt (1976) discussed different photosynthe- information on the symmetry and peakiness of a dis-
sis models that have been used to mathematically tribution (Armitage & Berry 1994). Additionally, the
describe oxygen production rates as a function of light Shapiro-Wilk W-test indicated normal distribution of
conditions (photosynthesis vs. irradiance, P/E, curves). the data (‘Analyse-it’ for Microsoft Excel). Hence, a
We tested 4 models to describe the experimental data: 2-way ANOVA was applied to test for differences
between the means of samples classified by the cate-
P B = Pmax αE /(Pmax + αE) Baly (1935)
gories of 2 factors (study site and season) (‘Analyse-it’
P B = Pmax tanh (αE /Pmax) Jassby & Platt (1976)
for Microsoft Excel). The model tested for the main
P B = Pmax [1 – exp (– αE /Pmax )] Webb et al. (1974)
effects of study site and season, as well as interactions
P B = Pmax [1 – exp (– αE /Pmax)] Walsby (1997)
between study site and season. When significant (p <
+ (E β) + R
0.05) effects were detected, an a posteriori comparison
where P B represents production rate at a given illumi- were made using Tukey’s test (‘Analyse-it’ for Micro-
nation, E; Pmax is maximum gross primary production soft Excel; Armitage & Berry 1994, Lozán & Kausch
rate under optimal light conditions (= photosynthetic 1998).
capacity); α is photosynthetic efficiency in the light-
limited part of the P/E curve; the Pmax:α ratio yields Ek,
which is an indicator of photosynthetic adaptation to RESULTS
prevailing light conditions; β is photoinhibition under
high light intensities; and R is respiration. Normalised Species composition
to chlorophyll a concentrations, the terms P Bmax and αB
will be used forthwith instead of the area-related terms For the eutrophic Kirr Bucht (KB), microscopic stud-
Pmax and α. ies revealed a phytoplankton community typical for
Adaptation of the models to the experimental data inner Bodden estuaries, with high diversity and little
was estimated by differences in the data obtained from seasonal variation. The following were the most com-
the fitted curve. The total error (sum of squared differ- monly found species (Pankow 1990, Lange-Bertalot
ences between the measured data and the fitted curve) 1998): Aphanocapsa sp., Aphanothece clathrata, Gom-
depends strongly on the absolute values of the photo- phosphaeria lacustris, G. pusilla, Merismopedia glauca,
synthetic rates. Thus, the total error was divided by the M. punctata, Microcystis aeruginosa and M. botrys
sum of the gross primary production rates of the fitted (Cyanophyceae: Chroococcales); Anabaena torulosa,
curve. In this way, the degree of adaptation of the dif- A. spiroides, Lyngbya contorta and Oscillatoria tenuis
ferent models to the experimental data was obtained (Cyanophyceae: Nostocales); Skeletonema costatum
for the different seasons and both study sites (data not (Bacillariophyceae: Centrales); Diatoma vulgare and
shown). The photosynthesis model of Webb et al. Surirella ovalis (Bacillariophyceae: Pennales); Botryo-
(1974) best described the experimental data. coccus braunii, Kirchneriella lunaris, Monoraphidium
Modelling. An interpolation of the data for times contortum, Oocystis pelagica, Pediastrum boryanum,
between experiments was achieved by applying P/E Scenedesmus sp. (7 species) and Tetrastrum triangu-
parameters and measured respiration rates to the lare (Chlorophyceae: Chlorococcales).
photosynthesis model of Walsby (1997) with the aid of In contrast, the phytoplankton community at the
constantly measured PAR data. Walsby’s (1997) model mesotrophic study site Rassower Strom (RS) resembled
considers not only PAR attenuation within the water the species composition of the offshore region (Arkona-
186 Aquat Microb Ecol 41: 181–198, 2005
see), with seasonal successions from diatom blooms in Cocconeis scutellum, C. placentula, Cymbella affinis,
spring to Cyanobacteria dominance in summer and Diploneis didyma, D. smithii, Epithemia turgida,
Dinophyceae development in autumn. The following Fragilaria sp., Navicula pygmaea, N. digitoradiata,
species were most abundant (Pankow 1990, Lange- Nitzschia compressa, N. constricta, Opephora sp.,
Bertalot 1998): Anabaena torulosa and Oscillatoria Pleurosigma sp., Surirella ovata). Thus, the species
tenuis (Cyanophyceae: Nostocales); Cyclotella comta, composition in the RS sediments differed clearly from
Chaetoceros danicus, Coscinodiscus radiatus, Melosira that in the water column.
sp., Skeletonema costatum and Stephanodiscus sp.
(Bacillariophyceae: Centrales); Gyrosigma sp., Pleuro-
sigma sp. and Surirella sp. (Bacillariophyceae: Pen- Pigment concentrations (chlorophyll a:phaeopigment a)
nales); Dinophysis sp., Gymnodinium sp., Peridinium
granii, Prorocentrum minimum and P. balticum (Dino- In the sediments of both study sites, highest chloro-
phyceae); Oocystis sp. and Pediastrum boryanum phyll a concentrations occurred mainly within the first
(Chlorophyceae: Chlorococcales). sediment horizon of 1 cm depth (seasonal range of 13
In the KB, Cyanobacteria (Chroococcales) and to 48 µg cm– 3 and 13 to 17 µg cm– 3 at KB and RS,
Chlorophyceae (Chlorococcales) dominated the algal respectively), and decreased with increasing sediment
community both on and within the sediment and in the depth (Fig. 2). In KB sediments, chlorophyll a concen-
water column, from where most species originated. trations were up to 9 times higher than the phaeopig-
Benthic pennate diatom species were found in low ment concentrations. In contrast, in the sediments at
abundances (Amphora sp., Cocconeis sp., Navicula RS, concentrations of active and degraded pigments
sp., Nitzschia sp., Surirella sp.). At the RS, a true micro- were similar. Sediments at KB contained up to 3 times
phytobenthos was established, with a high diversity of higher chlorophyll a concentrations than the sediments
pennate diatoms: Achnanthes delicatula, Amphora sp., at RS (Fig. 2).
0 S 0 S
-1 -1
-2 -2
-3 -3
Depth (cm)
-4 -4
-5 -5 Chl a RS
Phaeo a RS
-6 -6 Chl a KB
-7 -7 Phaeo a KB
-8 -8
-9 -9
A B
-10 -10
0 10 20 30 40 50 0 10 20 30 40 50
0 S 0 S
-1 -1
-2 -2
-3 -3
Depth (cm)
-4 -4
-5 -5
-6 -6
-7 -7
-8 -8
-9 -9
C D
-10 -10
0 10 20 30 40 50 0 10 20 30 40 50
Pigment concentration (µg cm-3) Pigment concentration (µg cm-3)
Fig. 2. Vertical profiles of chlorophyll a (chl a) and phaeopigment a (phaeo a) concentrations in sediments of Kirr Bucht (KB) and
Rassower Strom (RS) in (A) summer 1996, (B) autumn 1996, (C) winter 1997 and (D) spring 1997. Pigment detection began
in the flocculent layer on top of the sediment surface (S, ) and continued downwards to a depth of 10 cm
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 187
Photic zone (zPAR) intensities at the sediment surface, the peaks of photo-
synthetic activity moved downwards in the sediment.
According to the definition of the euphotic zone in In the sediments of RS, the highest gross production
the pelagic environment (Sommer 1998), the photic rates were always just beneath the sediment surface,
zone is defined as the sediment depth at which PAR e.g. zphot, spring, 0.8 mm RS; Fig. 4B), even with
is reduced to 1% of incident irradiance. Light inten- increasing incident irradiance (data not shown). The
sity and light penetration were measured using extension of the photosynthetic active zone as well as
spherical glass-fibre microsensors in the upper sedi- the gross primary production rates were significantly
ment horizons, which were exposed to various irra- higher in KB sediments than in RS sediments (p <
diances (Fig. 3). A clear light intensity peak was 0.0001; Table 2).
detected just below (Fig. 3A) and at (Fig. 3B) the
sediment surface; the peak was most pronounced at
higher light intensities. With increasing surface irra- Aerobic zone (zoxygen)
diance, the light penetrated significantly into deeper
sediment layers to a maximum depth beyond which In correlation with increasing incident irradiance,
increases in incident irradiances did not result in fur- the enhanced activity of photoautotrophic organisms
ther extension of the photic zone (Fig. 3). In the sandy led to higher oxygen production rates and an
sediments of KB, the photic zone was always more extended oxic layer in the upper sediment layers
pronounced than in the muddy sediments of RS (p < (Fig. 5). zoxygen is defined as the sediment depth at
0.0001, Table 2, Fig. 3). which 1 µmol l–1 of oxygen concentration is de-
Table 2. Mean ± SD (n = 3 to 10) oxygen consumption (O2consum: mmol O2 m–1 h–1)
Photosynthetic zone (zphot ) under dark conditions and extension (µm) of aerobic zone (zoxygen) under dark and
medium light conditions, and extension of photic layer (zPAR) and photosynthetic
Increasing irradiance at the sedi- active layer (zphot) under medium in situ light intensities in sediments of both study
sites at different seasons. nd: not determined
ment surface leading to deeper light
penetration into the sediment could
Date O2consum zoxygen zPAR zphot
activate photoautotrophic organisms Dark Dark Medium light Medium light Medium light
in deeper layers. Nevertheless, the
zone of photosynthetic activity did Kirr Bucht
not extend to the full extent of the 1 Jul 1996 –0.97 ± 0.24 1300 ± 400 1700 ± 150 2000 ± 150 800 ± 170
7 Oct 1996 –0.66 ± 0.19 1800 ± 150 3200 ± 150 3000 ± 400 1100 ± 300
photic zone (Table 2, Fig. 4). In 27 Jan 1997 –0.60 ± 0.08 2500 ± 150 6100 ± 210 1900 ± 000 nd
the sandy sediments of the KB, a 7 Apr 1997 .–120 ± 0.27 2400 ± 290 4700 ± 200 3200 ± 200 1600 ± 600
zone with pronounced photosynthetic Rassower Strom
activity was detected (e.g. spring, 8 Jul 1996 –0.89 ± 0.16 1600 ± 200 3500 ± 110 1800 ± 000 570 ± 60
1.6 mm), with several peaks of maxi- 30 Sep 1996 –0.79 ± 0.15 2300 ± 230 2600 ± 500 1600 ± 100 0100 ± 300
mal oxygen production in deeper 15 Jan 1997 –0.39 ± 0.06 3050 ± 230 2800 ± 250 1300 ± 000 nd
14 Apr 1997 –0.72 ± 0.15 3400 ± 220 6700 ± 140 1500 ± 150 0700 ± 100
layers (Fig. 4A). With increasing light
A 2 B 2
1 1
Depth (mm)
0
0
-1 1200
-1 900
1200 600
900 300
-2 600
300 -2 220
100
150
-3
60 -2 -1
-3
10
µE m s 60 µE m-2 s-1
-4 -4
0 200 400 600 800 1000 1200 1400 0 200 400 600 800 1000 1200 1400
PAR (µE m-2 s-1) PAR (µE m-2 s-1)
Fig. 3. Vertical light profiles in sediments of the (A) Kirr Bucht and (B) Rassower Strom, determined by a glass-fibre optical sensor
at different illumination intensities in autumn 1996. Horizontal line at depth zero marks the sediment surface, with the negative
values indicating sediment depth. PAR: photosynthetically active radiation
188 Aquat Microb Ecol 41: 181–198, 2005
2
GPP (nmol O2 cm-3 s-1) A
A 0 0.5 1.0 1.5 2.0 2.5 3.0 75
1 150
0 Surface 350
Depth (mm)
0
-0.4
-1
Depth (mm)
-0.8
-2 600
-1.2 900
-3 1200
2400 µE m2 s-1
-1.6
-4
0 200 400 600 800 1000 1200
-2.0
0 200 400 600 800 1000 1200 1400
O2-concentration (µmol l-1)
0 20 40 60 80 100 120 140 2
PAR (µE m-2 s-1)
B 75
150
1 350
Depth (mm)
GPP (nmol O2 cm-3 s-1) 0
0 0.5 1.0 1.5 2.0 2.5 3.0
B
0 -1
Surface
600
-2
-0.4 900
-3 1200
Depth (mm)
-0.8 µE m2 s-1
2400
-4
-1.2 0 100 200 300 400
O2 concentration (µmol l-1)
-1.6 Fig. 5. Vertical oxygen profiles in sediments of the (A) Kirr
Bucht and (B) Rassower Strom, determined by the oxygen
-2.0 Clark-type microelectrode under different illumination inten-
0 200 400 600 800 1000 1200 1400 sities in autumn 1996. Further details as for Fig 3
O2-concentration (µmol l-1)
0 20 40 60 80 100 120 140
PAR (µE m-2 s-1)
Oxygen consumption and net primary production
Fig. 4. Gross primary production, GPP (bars), oxygen concen-
trations and PAR at different sediment depths at medium
in situ light intensity in spring 1997 at (A) Kirr Bucht and At both study sites, oxygen consumption and net
(B) Rassower Strom primary production within the sediments (determined
under dark and light conditions, respectively) showed
a clear seasonal trend, with lowest rates in winter
tectable. According to this definition, oxygen micro- (Table 2, Fig. 6). Oxygen consumption and net primary
profiles indicated an extension of the aerobic zone of production rates within the sandy KB sediments were
1.3 to 2.5 mm and 1.6 to 3.4 mm (seasonal range; both significantly higher than in the muddy RS sedi-
Table 2) in dark conditions in the sediments of the ments (p < 0.0001; Table 2, Fig. 6). Nevertheless, the
KB and RS, respectively (differences between the ratios of gross oxygen production:oxygen consump-
study sites were significant at the level p < 0.0003). tion, representing photoautotrophic and heterotrophic
Even under illumination, the extension of zoxygen was processes (omitting for the latter the chemical oxygen
still higher in the RS sediments than in the KB sedi- demand in the sediment), were much higher in KB
ments in spring and summer (p < 0.0001; Table 2). than RS, and most pronounced under the highest natu-
Nevertheless, the higher benthic microalgal biomass rally occurring light intensities (seasonal range: KB,
and photosynthetic rates at KB resulted in up to 6 5 to 10; RS, 0.8 to 4). Nevertheless, the oxygen pro-
times higher maxima of oxygen concentrations in the duction in the RS sediments was sufficient to meet the
upper sediment layers of KB compared to RS (p < oxygen demand even at low light intensities (except in
0.0001; Figs. 4 & 5). winter), as indicated by the positive oxygen net fluxes.
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 189
0.7 A 2.0
A
0.6
GPP (mg C mg-1 chl a h-1)
1.5
0.5
NPP (µmol O2 cm-2 h-1)
0.4
1.0
0.3
July 1996, r = 0.84
0.5
0.2 October 1996, r = 0.99
April 1997, r = 0.96
0.1 January 1997, r = 0.98
0
0 500 1000 1500 2000 2500
0.0
–0.1 B 2.0
0.7
B
GPP (mg C mg-1 chl a h-1)
1.5
0.6
0.5
NPP (µmol O2 cm-2 h-1)
1.0
0.4
July 1996, r = 0.84
0.3 0.5
October 1996, r = 0.99
April 1997, r = 0.96
0.2 January 1997, r = 0.98
0
0.1 0 500 1000 1500 2000 2500
PAR (µE m-2 s-1)
0.0
Fig. 7. Seasonal photosynthesis/irradiance (P/E) curves for
microphytobenthos in (A) Kirr Bucht and (B) Rassower Strom
–0.1
L M H L M H L M H L M H sediments calculated according to the model of Webb et
Jul 1996 Sep 1996 Jan 1997 Apr 1997 al. (1974)
Fig. 6. Mean (± SD) net primary production (NPP) of micro-
phytobenthos in sediments of the (A) Kirr Bucht and (B) Ras-
both sites, the maximal primary production rates fol-
sower Strom, at different in situ light intensities (L: low;
M: medium; H: high) in different seasons lowed seasonal changes in temperature (r = 0.82 and
0.71) and mean light intensities (r = 0.85 and 0.76) (KB
and RS, respectively). The α B values, reflecting photo-
Gross primary production synthetic efficiency, showed negative correlations with
The areal gross primary production rates were sig- Table 3. Parameters of photosynthesis/irradiance (P/E)
nificantly higher at KB than RS (p = 0.0282). Nor- curves; data normalised to chlorophyll a (chl a), showing
photosynthetic efficiency, αB (mg C mg–1 chl a) h–1 (µE m–2
malised to chlorophyll a, the gross primary produc- s–1)–1, maximum photosynthetic capacity, P Bmax (mg C mg–1
tion rates were still slightly higher in winter in the chl a h–1), and light saturation, Ek (µE m–2 s–1) related to
KB sediments than in the RS sediments, but were microphytobenthic primary production for both study sites
comparable in summer at the 2 sites (Fig. 7). In in different seasons
autumn 1996 and spring 1997, the specific produc-
tion rates were significantly higher in the sediments Kirr Bucht Month Rassower Strom
αB P Bmax Ek αB P Bmax Ek
of RS (p < 0.0001).
The P Bmax values, reflecting photosynthetic capacity 0.0096 1.46 152 Jul 1996 0.0133 1.54 116
under prevailing light conditions, showed a clear sea- 0.0123 0.66 54 Sep/Oct 1996 0.0121 1.28 106
sonal trend in KB sediments, but the trend was less 0.0131 0.29 22 Jan 1997 0.0171 0.17 10
0.0124 0.40 32 Apr 1997 0.0189 1.63 86
pronounced for RS (Table 3, Fig. 7). Nevertheless, at
190 Aquat Microb Ecol 41: 181–198, 2005
temperature (r = 0.75 and 0.82) and mean light condi- Contribution of benthic primary production
tions (r = 0.81 and 0.76) (KB and RS, respectively).
Thus, light saturation Ek , defined as the ratio P Bmax:α B, Since net oxygen production and respiration rates
correlated with both temperature (r = 0.77 and 0.93) can be derived from oxygen microprofiles for sediments
and mean light intensity (r = 0.82 and 0.94) (KB and RS, only, pelagic primary production was determined by
respectively). the oxygen exchange method. The interpolation of the
measured benthic and pelagic primary production rates
over 24 h for those days on which measurements were
The benthic habitat — sink or source of oxygen? made showed that the microphytobenthos contributed
from 26 to 59% and 2 to 53% to the total primary pro-
On the basis of the foregoing (R, α B, P Bmax), and duction at KB and RS, respectively. The relative contri-
linked with respiration rates and the results of con- bution of benthic primary production was highest in
stant PAR measurements, the model of Walsby (1997) spring at both sites. A further interpolation of the mea-
allowed interpolation of the net primary production sured data with constantly determined PAR values and
rates for the time intervals between measurements. the Walsby (1997) model over the course of 1 yr showed
This was initially performed for the 24 h of each sam- that, as an annual average, the microphytobenthos ac-
pling day in the different seasons. Whereas for the 8 h counted for 37 and 30% of the total primary production
illumination a positive oxygen flux was calculated at KB and RS, respectively (Fig. 9). The carbon fixation
even in the low light range at both study sites (except rates by the microphytobenthos were calculated as 2 to
in winter at RS: Fig. 6), daily calculation of the oxygen 17 g C m–2 mo–1 (113 g C m–2 yr–1) for KB (Fig. 9A) and
budget indicated negative oxygen fluxes in summer 0.2 to 7 g C m–2 mo–1 (42 g C m–2 yr–1) for RS (Fig. 9B).
and autumn for RS and in winter for KB (Fig. 8). For The pelagic gross production rates, integrated over the
both study sites, integrated over 24 h, the highest pos- water depth, were 2 times higher in the shallow KB (5 to
itive oxygen fluxes for the benthic habitat were calcu- 30 g C m–2 mo–1, 190 g C m–2 yr–1) than in the deeper RS
lated for spring. (2 to 24 g C m–2 mo–1, 108 g C m–2 yr–1) (Fig. 9).
5 5
KB + 14.1 mmol O2 m-2 d-1
4
A KB + 5.4 mmol O2 m-2 d-1
4
B RS – 10.3 mmol O2 m-2 d-1
NPP (mmol O2 m-2 h-1)
RS – 8.6 mmol O2 m-2 d-1
3 3
2 2
1 1
0 0
–1 –1
–2 –2
0 2 4 6 8 10 12 14 16 18 20 22 24 0 2 4 6 8 10 12 14 16 18 20 22 24
5 5
C KB + 0.8 mmol O2 m-2 d-1
D
NPP (mmol O2 m-2 h-1)
4 RS – 11.7 mmol O2 m-2 d-1 4
3 3
2 2
1 1
0 0
–1 –1 KB + 20.6 mmol O2 m-2 d-1
RS – 2.7 mmol O2 m-2 d-1
–2 –2
0 2 4 6 8 10 12 14 16 18 20 22 24 0 2 4 6 8 10 12 14 16 18 20 22 24
Time (h-1) Time (h-1)
Fig. 8. Benthic net primary production (NPP), interpolated using Walsby’s model (1997), over the days on which sampling was
carried out (see Table 2) in Kirr Bucht and Rassower Strom sediments in different seasons. (A) summer 1996; (B) autumn 1996;
(C) winter 1997; (D) spring 1997
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 191
30 100 Microphytobenthos: light climate and
A species composition
25
80
In recent decades, the nutrient load of
20 municipal, agriculture and industrial water
60 has led to an increase in phytoplankton bio-
15 mass in the Bodden (Wasmund & Schiewer
40
1994, Schiewer 1998), resulting in drastic
10 changes in the underwater light field.
Phytoplankton adds significantly to the
% of MPB on total GPP
20 scattering and absorption of light in the
GPP (mg C m-2 mo-1)
5
water column reducing light intensity and
0 0 altering the spectral composition (Schubert
et al. 2001, S. U. Gerbersdorf unpubl.).
Thus, water transparency at the eutrophic
30 100
study site, Kirr Bucht, was 4 to 6 times lower
B than at the mesotrophic study site, Ras-
25
80 sower Strom. Nevertheless, at the sediment
surface, light availability (the main abiotic
20 factor influencing microphytobenthic pho-
60
tosynthesis) was similar in both areas due to
15 different morphologies and water depths
40 (KB, 0.6 m; RS, 3.4 m). However, the species
10 composition of the benthic algae differed
qualitatively at the 2 sites. Microscopic
20
5 investigation revealed that Cyanobacteria
of the order Chroococcales and Chloro-
0 0 phyceae of the order Chlorococcales were
ry ry h ril y e y st r r r r
nua brua Marc Ap Ma Jun Jul ugu mbe tobe mbe mbe dominant on the sediment surface of KB;
Ja Fe A pte Oc ove ece
Se N D with a similar composition of species (e.g.
Fig. 9. Carbon fixation rates (gross primary production, GPP) for the Gomphospheria lacustris, Merismopedia
benthal (black bars) and the pelagial (grey bars), interpolated using the punctata, Scenedesmus quadricauda and
Walsby model (1997) on a monthly basis, in the (A) Kirr Bucht and Oocystis sp.) in the water column. Only a
(B) Rassower Strom. Curve indicates contribution of photosynthetic few benthic diatoms such as Gyrosigma
activity of the microphytobenthos (MPB) to total GPP
balticum and Surirella sp. were present in
KB sediments, indicating that most of the
‘microphytobenthos’ originated from the
DISCUSSION overlying water column. In contrast, the species
composition in the sediment and water column clearly
The significance of microphytobenthic primary differed at RS. The microphytobenthos at RS mainly
production for the aquatic habitat is obvious (Koop et consisted of pennate diatoms such as Navicula sp. and
al. 1990, Rizzo 1990, Wiltshire 1992, Berninger & Amphora sp. However, in terms of oxygen and carbon
Epstein 1995, MacIntyre & Cullen 1996, MacIntyre et supply, the sedimented pelagic algae in the KB are
al. 1996, de Brouwer et al. 2003). Nevertheless, only comparable to an actual microphytobenthos; thus, we
some 100 papers in the last few decades have exam- have used the term ‘microphytobenthos’ for both study
ined the subject of microphytobenthos on a global sites.
scale, and even fewer have investigated the sublit-
toral zone. Until recently (Meyercordt et al. 1999,
Gerbersdorf 2000, Gerbersdorf et al. 2004), almost no Highly resolved measurements in the sediment
investigations on the microphytobenthos had been
carried out in the Bodden areas of the southern Microelectrode studies are mainly known from the
Baltic Sea. The present study examined microphyto- intertidal zone (e.g. Barranguet et al. 1998) or within
benthic primary production in 2 Bodden areas differ- microbial mats (e.g. Oren et al. 1995) and the investi-
ing in trophic status, and thus in conditions for the gations presented here are the first to use micro-
microphytobenthos. sensors in the Bodden estuaries. The microsensors
192 Aquat Microb Ecol 41: 181–198, 2005
provided very detailed information on the spatial and oxygen penetration not only under dark conditions,
temporal heterogeneity of light, photosynthetic activ- but also under illumination in spring and summer.
ity and oxygen within the sediment itself. The sedi- The question remains as to whether the higher oxygen
ments at both study sites had different soil charac- supply in KB sediments leads to enhanced microbial
teristics, which altered the light climate within the processes, as indicated by the relatively high ratio of
sediment in predictable ways. The photic zone (zPAR) active and degraded pigments, or whether a greater
in the sandy sediments of KB was about twice as deep supply of fresh organic material through primary pro-
(seasonal range 1.4 to 3.2 mm) as that in the muddy duction may have led to the higher oxygen consump-
sediments of RS (seasonal range 0.9 to 2.0 mm) under tion rates in the KB sediments. More important is
in situ light intensities. This was in agreement with the opportunity (now provided by microsensors) to
the findings of Jørgensen & des Marais (1990) and examine the varying penetration of zoxygen in seasonal
Kühl et al. (1994), who determined a photic zone of terms and its consequences in the sediments of both
1.3 to 4.6 and 0.2 to 2.0 mm for sandy and muddy sed- study sites.
iments, respectively. Light attenuation is determined
mainly by absorption, which is stronger in sediments
with higher organic content. If absorption is low, Significance of microphytobenthos
strong scattering can retain a high light intensity at a
given depth; this is especially enhanced near optical The occurrence of many organisms is determined by
boundaries, resulting in maximum scalar irradiance. the aerobic conditions within the sediment. Thus, the
This was seen within the first 1 mm of the strongly highest abundance and vertical distribution of meio-
scattering, sandy sediment of KB, leading to peaks in fauna (Arlt & Georgi 1999), heterotrophic flagellates
light intensity of up to 140% relative to incident light and amoebae (Garstecki et al. 1999) as well as bacteria
from above (up to 200% in sandy sediments in- (Rieling 1999) (determined simultaneously in parallel
vestigated by Kühl et al. 1994 and Oren et al. 1995). investigations) matched the expansion of the aerobic
In contrast, in RS sediments, pronounced light inten- zone at both study sites. In anoxic layers, sulphate-
sity peaks occurred directly at the sediment surface reducing bacteria became dominant in the sediments
due to scattering and reflection. In agreement with lit- of both study sites (Babenzien & Voigt 1999). Further-
erature data, the light attenuation coefficient for the more, the importance of the aerobic layer to redox
first 5 mm sediment layer was much lower in the conditions and nutrient fluxes was shown by the
sandy sediments of KB than in the muddy sediments release of manganese and iron (Stodian et al. 2000)
of RS (seasonal k range of 0.4 to 1.0 mm–1 and 1.3 to and the release of o-phosphate and ammonia (Rieling
2.0 mm–1, respectively). et al. 2000) under anoxic conditions, whereas these
Under in situ irradiances, the photosynthetic active compounds are bound to the sediment in oxidised
zone (zphot) ranged down to a maximum of 2 mm form. The microphytobenthos also assimilates nutrients
depth in KB sediments, but to a maximum depth of for photosynthetic activity, thereby reducing the
only 1 mm in RS sediments, as measured by the nutrient fluxes of o-phosphate and ammonia under
light/dark shift method. Consequently, zphot did not illumination significantly (Gerbersdorf et al. 2000, Riel-
resemble zPAR at either study site. Presumably, less ing et al. 2000).
than 20 µE m–2 s–1 was not sufficient to support the Initiated by illumination, migration towards the sur-
photosynthetic activity of the pelagic species in the face and photosynthetic activity of the algae lead to
KB sediments. At the same time, the pennate diatoms stabilisation of the sediment along with mat formation
in RS sediments could migrate to upper layers with and EPS (extracellular polymeric substances) produc-
better light availability. Despite a generally more tion/excretion (S. U. Gerbersdorf unpubl.). This is im-
extensive zPAR in KB sediments, zphot at this site was portant in shallow waters, where even low winds can
significantly more pronounced only in spring com- otherwise lead to resuspension events (Schnese 1973).
pared to RS. Nevertheless, at KB, 3 times higher pig- With regard to the benthic–pelagic coupling, micro-
ment concentrations in the upper 0.5 cm (up to 50 µg benthic algae can contribute not only to the oxygen
cm– 3) resulted in significantly higher rates of photo- and carbon supply within the sediment, but also to that
synthetic activity and up to 6 times higher oxygen in the water column through resuspension processes
concentrations in the upper layers compared to RS (Schiewer 1998). Therefore, in addition to investigating
(maximum of 1100 and 300 µmol l–1, respectively). the spatial and temporal heterogeneity of the meta-
This did not necessarily lead to a higher oxygen pen- bolic processes within the sediment itself, we exam-
etration in KB sediments, as the oxygen consumption ined the primary production of the microphytobenthos
there was generally higher than in RS sediments. as one of the main driving forces in the carbon budget
Consequently, the muddy RS sediments had higher of these shallow waters.
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 193
Primary production of microphytobenthos Physiological adaptations of microphytobenthos
The high benthic chlorophyll a concentrations in Over the course of the year, photosynthetic rates var-
the KB sediments reflected the high biomass of ied not only as a function of biomass, but also (strongly)
phytoplankton at this eutrophic site, which was as a function of abiotic factors (temperature, r = 0.82
deposited on the sediment surface. Under in situ and 0.71; light, r = 0.85 and 0.76, for KB and RS, respec-
light conditions, the benthic gross primary produc- tively), in accordance with reports in the literature (e.g.
tion rates in KB sediments (28 to 80 mg C m–2 h–1) Blanchard & Guarini 1996). Temperature affects the
were 3 times higher than in RS. Thus, benthic pri- specific activities of enzymes (Epping 1996), which in
mary production rates in KB sediments were well turn affect C-assimilation as well as the electron trans-
within the range of data for highly productive diatom port chain (Kohl & Nicklisch 1988). Light intensity
associations in the Wadden Sea. Colijn & de Jonge determines photosynthetic capacity by influencing the
(1984) and Barranguet et al. (1998) determined orientation, size and number of reaction centres and
benthic gross production rates of 10 to 115 mg C m–2 the capacity of the Calvin cycle (Kohl & Nicklisch
h–1 and 11 to 58 mg C m–2 h–1 in the tidal zone, 1988). Since temperature and light were comparable at
respectively, depending on season. Moreover, the the sediment surface of both study sites, no significant
photosynthetic rates in KB sediments at light intensi- differences in the physiological adaptations of the 2
ties up to 350 µE m–2 s–1 were 1.5 times higher than algal communities would be expected. Nevertheless,
in biofilms along an eutrophication gradient in Bod- the parameters of the P/E curves such as photosyn-
den waters (34.4 to 94.5 mg C m–2 h–1 at radiation thetic capacity (Pmax), photosynthetic efficiency (α) and
levels of 100 to 800 µE m–2 s–1, Meyer-Reil & Neu- light saturation (Ek), should indicate general adapta-
dörfer 1998). In contrast, RS sediments had primary tions of the benthic algae to, for example, low light
production rates (3 to 36 mg C m–2 h–1) that were regimes when data from both study sites are compared
comparable with data obtained for deeper sublittoral with data in the literature (Kohl & Nicklisch 1988,
coastal areas. Gargas (1972) and Herndl et al. (1989) Pickney & Zingmark 1991, Falkowski & Raven 1997,
determined gross primary production rates of 0.5 to Barranguet et al. 1998).
21 mg C m–2 h–1 at 4 m depth and 10 to 13 mg C m–2 Normalised for chlorophyll a, the P Bmax, maximum
h–1 at 7 to 22 m depth, respectively. Nevertheless, photosynthetic values were (except for winter) lower
the microphytobenthos at RS displayed as much as for KB benthic microalgae than for those at RS, although
half of the photosynthetic activity measured in the medium light availability at the sediment surface
biofilms in Bodden waters (Meyer-Reil & Neudörfer was comparable or even higher at KB. This could indi-
1998), although biofilms are usually known as sys- cate nutrient limitation at times of high photosynthetic
tems with high metabolic activities. activities in the sediment, as described by Sundbäck
In regard to a possible decline in the microphyto- & Snoeijs (1991), although usually nutrient limitation
benthos due to eutrophication, excessive phyto- in the benthic habitat is less likely because benthic
plankton development and decreasing light avail- microalgae can assimilate nutrients directly out of the
ability at the sediment surface, comparison of our interstitial water (Shaffer & Onuf 1983). Also, the high
data with earlier findings at the 2 study sites would benthic algal biomass in the upper layers of the KB
have been of particular interest. Unfortunately, no sediments could have shaded the algae in deeper
data for RS and only a few earlier publications for KB layers, resulting in lower mean photosynthetic capac-
are available for microphytobenthic primary produc- ity rates integrated over the depths measured. Mac-
tion. Wasmund (1986) measured benthic primary Intyre & Cullen (1996) demonstrated higher P Bmax val-
production in a similar range to our data (7 to ues in the upper than the lower sediment depths (6 to
117 mg C m–2 h–1), but the sediments he investigated 10 compared to 0.6 to 2.8 mg C mg–1 chl a h–1) as a
originated from a depth of only 15 to 20 cm, which is result of adaptation to different light conditions. The
much less than the water depth at our study site. It is P Bmax values in the present paper were in the range of
not feasible to discuss the decline in microphyto- 0.17 to 1.63 mg C mg–1 chl a h–1 at both study sites and
benthos using the few data currently available, thus comparable to data from other sublittoral offshore
especially considering the well-known variations in regions. Plante-Cuny & Bodoy (1987) determined P Bmax
primary production rates that can occur within a few of 0.46 to 1.23 mg C mg–1 chl a h–1 in sandy sediments
hours even at the same investigation point (Blan- at 0.5 m depth in the Golfe de Fos, France. In the
chard et al. 2001). Monitoring programmes are Wadden Sea, the algae experience temporally higher
strongly recommended to reveal possible effects of light intensities and temperature, resulting in higher
eutrophication on the microphytobenthos on a long- chlorophyll-specific production rates. Thus, Pickney &
term basis. Zingmark (1991) reported variation in P Bmax between
194 Aquat Microb Ecol 41: 181–198, 2005
0.27 and 4.42 mg C mg–1 chl a h–1, with highest values sen for our measurements to be representative for both
at low tide. Barranguet et al. (1998) measured photo- locations. Accordingly, the KB sediments could be a
synthetic capacity of up to 13 mg C mg–1 chl a h–1 in source of oxygen except in wintertime, and the RS sed-
tidal areas of the Dutch Wadden Sea. iments mainly a sink of oxygen except from late spring
Together with the αB values, which indicate the to summer.
photosynthetic efficiency of photon utilisation, the
photosynthetic capacity, P Bmax determines the light
saturation value Ek, an indicator for photosynthetic Contribution of microphytobenthos to total
acclimatisation to prevailing light conditions. In gen- primary production
eral, relatively low Ek is expected under low light
conditions, when benthic microalgae utilise the photon To estimate the significance of microphytobenthic
flux more efficiently (relatively high αB) and achieve primary production in relation to total primary produc-
maximal photosynthetic activity quite quickly (rela- tion, the pelagic primary production rates must be
tively low P Bmax). As for P Bmax, αB and Ek were corre- taken into consideration. Because microelectrodes can
lated with temperature and light conditions at both only be used in the sediment, the photosynthetic activ-
study sites over the course of the year (P Bmax and Ek ity of phytoplankton was determined by the oxygen
positively, αB negatively). The seasonal Ek values exchange method. Both methods are well-fitted to the
ranged from 22 to 152 µE m–2 s–1 and from 10 to 116 µE nature of the relevant samples (pelagic production–ex-
m–2 s–1 for KB and RS, respectively, and reflected adap- change method for oxygen development and detection
tations of the microalgae to rather low light conditions within the water, benthic production–microelectrodes
at both study sites. This agrees with data in the litera- method for oxygen development and detection within
ture, which cover a broad range of light saturation the sediment) and thus, little difference resulting from
values (e.g. Robinson et al. 1995, McMurdo Sound, methodology was expected between the data sets for
Antarctica: 1.3 to 4.5 µE m–2 s–1; Whitney & Darley pelagic and benthic primary production. For sediment
1983, sand bank in Georgia: 2044 µE m–2 s–1). The Ek samples, microelectrodes gave much more reliable
values in the present paper were comparable to values results on benthic primary production than more inte-
for the tidal zone during high tide reported by Colijn & grative methods such as oxygen exchange measure-
Van Buurt (1975), where the turbidity of the water ments. Microelectrodes measure photosynthetic activ-
column led to high light attenuation and mean Ek ity directly at the production spot within the sediment,
values of 165 µE m–2 s–1. and both upward and downward oxygen fluxes are
included (Revsbech et al. 1981). Hence, gross benthic
primary production rates calculated on a monthly basis
The benthic habitat — sink or source of oxygen? in the present paper (KB: 2 to 17 g C m–2 mo–1; RS: 0.2
to 7 g C m–2 mo–1) were on average 2 times higher than
Under medium to maximum in situ light intensities, those reported by Meyercordt & Meyer-Reil (1999),
maximum photosynthetic capacity of the microphyto- who used the oxygen exchange method. The differ-
benthos was achieved at all seasons and at both study ences in benthic primary production rates determined
sites. The resulting photosynthetic oxygen production by both methods were more pronounced under the low
was able to meet the oxygen demand of the sediment, light regime, where oxygen production was at or
as indicated by positive oxygen fluxes at both study below the detection limit of the oxygen exchange
sites and at all seasons investigated, except in winter approach (Gerbersdorf 2000).
at RS. Nevertheless, the benthic microalgae only expe- Benthic and pelagic primary production rates were
rienced these irradiances during approximately 8 h of interpolated over the days on which sampling was
total illumination around noon on an annual average. carried out. On these days, the microphytobenthos
Applying the model of Walsby (1997), the data on oxy- accounted for about 26 to 59 and 2 to 53% of the total
gen consumption and production were interpolated primary production in KB and RS, respectively. The
over 24 h for the various sampling days (see Table 2) highest contribution (> 50%) to primary production by
using the determined respiration rates, P/E, and the the benthic algae was for spring, corresponding with
constantly measured PAR values. The daily oxygen the best light conditions at the sediment surface, while
budget of the benthic habitat (integrating dark and the lowest contribution (19 to 26%) was for summer
light periods) displayed negative oxygen fluxes for RS (except for winter at RS, where their contribution was
sediments in January, July and October and for KB exceptionally low), corresponding with low light avail-
sediments in January. Although photosynthetic activ- ability on that particular sampling day. In regard to the
ity and the light field are highly dynamic, interpolation high variability in the light field, the interpolation of
of the data on a monthly basis revealed the days cho- data on a monthly basis allowed more general con-
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 195
clusions as to the significance of microphytobenthic aries. The contribution of the benthic microalgae in
photosynthetic activities in the aquatic environment. terms of total primary production is substantial, and be-
Again, the lowest ratio of pelagic to benthic primary cause of the higher sensitivity of the detection method
production was for early spring, when the chlorophyll used (microelectrodes as opposed to the oxygen-
a concentrations in the water column indicated a 30% exchange method), even higher than that reported in
lower phytoplankton biomass resulting in a better light former publications. Taking into account the different
availability at the sediment surface compared to sum- water depths and water transparencies at the 2 study
mer and autumn. During the course of the year, the sites (eutrophic/mesotrophic status), the negative im-
contribution of the microphytobenthos to total primary pact of nutrient load and enhanced light attenua-
production was substantial and comparable at both tion caused by excessive phytoplankton development
study sites (37 and 30% for KB and RS, respectively). on microphytobenthic photosynthetic activity was re-
This can be explained by the morphology (water depth vealed. A true microphytobenthos was established at
at KB = 0.6 m, at RS = 3.4 m) and hydrography (light the mesotrophic study site, while pelagic algae species
attenuation at KB k = 3.17 m–1, at RS k = 0.61 m–1), at dominated on the sediment surface at the eutrophic
the 2 sites, which produced a similar light climate at site. A shift in benthic microalgal species composition
the sediment surface of both areas. Only by calculating could have serious consequences such as effects on
the benthic primary production for varying water productivity (different photon flux efficiencies) or sedi-
depths and taking into account the different water ment stability (differential EPS production). Although
transparency at each site could the effect of eutrophi- the input of sewage into rivers and coastal areas has
cation be revealed. been significantly reduced over the last few decades
(e.g. through the construction of numerous sewage
treatment plants), the internal load of nutrients within
Effects of trophic status the sediment (i.e. ‘legacy of the past’) remains a prob-
lem. Hence, monitoring programmes are still neces-
Because of the turbid and phytoplankton-rich water sary to assess the risks and evaluate possible effects of
column in the eutrophic KB, no light would be avail- eutrophication on the aquatic environment and enable
able at the sediment surface with a theoretical water development of appropriate remediation strategies in
depth of 3.4 m (the actual depth of the RS site), and endangered areas.
thus, no benthic photosynthetic activity would be pos-
sible there. In contrast, at the mesotrophic RS, signifi- Acknowledgements. The authors thank the crew of RV ‘Pro-
cant benthic primary production was measured at this fessor Fritz Gessner’ for assistance during sampling and Mar-
ion Köster, Ingrid Kreuzer, Frank Neudörfer, Georg Schubert,
water depth over the course of the year, except in win-
Joachim Timm and Wolfgang Zenke for excellent technical
ter. Based on a common depth of 0.6 m (the actual support. The authors are grateful to Helmut Hübel and
depth of the KB site), the benthic primary production Kirsten Wolfstein for enthusiastic teaching and help in the de-
rates would be similar at both study sites (Meyercordt termination of algal species. The investigations presented
& Meyer-Reil 1999), despite much less benthic micro- here were part of the joint research project ‘ÖKOBOD’ (Öko-
system Boddengewässer — Organismen und Stoffhaushalt) fi-
algal biomass at the RS. Assuming a common water nanced by the German BMBF (Bundesministerium für Bil-
depth of 2 m, resembling the mean water depth of the dung, Wissenschaft Forschung und Technologie).
Bodden, Meyercordt et al. (1999) showed that the
microphytobenthos would support 30 to 45% of the LITERATURE CITED
total primary production at RS, but only ≤0.3% at KB.
These calculations all support the hypothesis that Arlt G, Georgi F (1999) Meiofauna in der bentho–pelagischen
eutrophication coupled with excessive phytoplankton Kopplung. In: Black HJ, Köster M, Meyer-Reil LA (eds)
Ökosystem Boddengewässer — Organismen und Stoff-
development and decreasing light availability at the
haushalt (ÖKOBOD), BMBF. Abschlußbericht, Verbund-
sediment surface has strong negative impacts on projekt, Bodden 8. Institut für Ökologie der EMAU Greifs-
microphytobenthic primary production. wald, Kloster/Hiddensee, p 19–24
Armitage P, Berry G (1994) Statistical methods in medical
research. Blackwell Scientific, Oxford
Babenzien HD, Voigt A (1999) Bedeutung der Sulfatreduktion.
CONCLUSION In: Black HJ, Köster M, Meyer-Reil LA (eds) Ökosystem
Boddengewässer — Organismen und Stoffhaushalt (ÖKO-
The present study has shown the significance of the BOD), Abschlußbericht, Verbundprojekt, Bodden 8. Insti-
microphytobenthos for the oxygen supply and carbon tut für Ökologie der EMAU Greifswald, Kloster/Hidden-
see, p 67–72
budget of the benthic habitat (and, via resuspension,
Bachor A, von Weber M, Wiemer R (1996) Die Entwicklung
to the pelagic environment also), as evidenced by its der Wasserbeschaffenheit der Küstengewässer Mecklen-
primary production rates in the shallow Bodden estu- burg-Vorpommerns. Nährstoffeinträge aus Mecklenburg-
196 Aquat Microb Ecol 41: 181–198, 2005
Vorpommern in die Ostsee 1990–1995. Wasser Boden 48: ham SA (1999) Trophische Beziehungen innerhalb benthi-
26–36 scher mikrobieller Nahrungsgewebe. In: Black HJ, Köster
Baly ECC (1935) The kinetics of photosynthesis. Proc R Soc M, Meyer-Reil LA (eds) Ökosystem Boddengewässer — Or-
Lond Ser 117:218-239 ganismen und Stoffhaushalt (ÖKOBOD), Abschlußbericht,
Barnett PRO, Watson J, Connelly D (1984) A multiple corer for Verbundprojekt, Bodden 8. Institut für Ökologie der EMAU
taking virtually undisturbed samples from shelf, bathyal Greifswald, Kloster/Hiddensee, p 29–38
and abyssal sediments. Oceanol Acta 7:339–409 Gerbersdorf SU (2000) Die pelagische und mikrophytoben-
Barranguet C, Kromkamp J, Peene J (1998) Factors control- thische Primärproduktion in den Boddengewässern unter
ling primary production and photosynthetic characteris- Berücksichtigung der Sedimentauflage, ihrer Fraktionen
tics of intertidal microphytobenthos. Mar Ecol Prog Ser und Aggregate. PhD dissertation, Universität Greifswald
173:117–126 Gerbersdorf SU, Meyercordt J (1999) Primärproduzierende
Behrens J (1982) Soziologische und produktionsbiologische Prozesse in Pelagial und Benthal. In: Black HJ, Köster M,
Untersuchungen an submersen Pflanzengesellschaften Meyer-Reil LA (eds) Ökosystem Boddengewässer —
der Darß-Zingster Boddengewässer. PhD dissertation, Organismen und Stoffhaushalt (ÖKOBOD), Abschluß-
Universität Rostock bericht, Verbundprojekt, Bodden 8. Institut für Ökologie
Berninger UG, Epstein SS (1995) Vertical distribution of der EMAU Greifswald, Kloster/Hiddensee, p 39–47
benthic ciliates in response to the oxygen concentration Gerbersdorf SU, Black HJ, Meyercordt J, Meyer-Reil LA,
in an intertidal North Sea sediment. Aquat Microb Ecol Rieling T, Stodian I (2000) Significance of microphytoben-
9:229–236 thic primary production in the Bodden (southern Baltic
Blanchard GF, Guarini JM (1996) Studying the role of mud Sea). In: Flemming BW, Delafontaine MT, Liebezeit G
temperature on the hourly variation of the photosynthetic (eds) Muddy coasts dynamics and resource management.
capacity of microphytobenthos in intertidal areas. C R Proc Mar Sci, Vol 2. Elsevier Science BV, Amsterdam,
Acad Sci Sér III Sci Vie 319:1153–1158 p 127–136
Blanchard GF, Guarini JM, Orvain F, Sauriau PG (2001) Gerbersdorf SU, Meyercordt J, Meyer-Reil LA (2004) Micro-
Dynamic behaviour of benthic microalgal biomass in phytobenthic primary production within the flocculent
intertidal mudflats. J Exp Mar Biol Ecol 264:85–100 layer, its fractions and aggregates, studied in two shallow
Börner R, Kell V (1982) Einfluß von Nährstoffanreicherungen Baltic estuaries of different eutrophic status. J Exp Mar
auf die Biomasse, Artensequenz und Primärproduktion Biol Ecol 307:47–72
des Phytoplanktons während einer Komplexanalyse im HELCOM (Helsinki Commission) (1988) Guidelines for the
Zingster Strom (Juni 1981). Wiss Z Wilhelm-Pieck-Univ Baltic Monitoring Programme for the third stage. Loose
Rostock Math-Natwiss Reihe 31:53–56 sheet version of the Baltic Sea Environment Proceedings
Burris JE (1981) Effects of oxygen and inorganic carbon con- No. 27D. Helsinki Commission, Helsinki, p 1–60
centrations on the photosynthetic quotients of marine Herndl GJ, Peduzzi P, Fanuko N (1989) Benthic community
algae. Mar Biol 65:215–219 metabolism and microbial dynamics in the Gulf of Trieste
Cadée GC, Hegeman J (1974) Primary production of the ben- (Northern Adriatic Sea). Mar Ecol Prog Ser 53:169–178
thic microflora living on tidal flats in the Dutch Wadden Hübel H (1968) Die Bestimmung der Primärproduktion des
Sea. Neth J Sea Res 8:260–291 Phytoplanktons der Nordrügenschen Boddenkette unter
Colijn F (1982) Light absorption in the waters of the Ems- Verwendung der Radiokohlenstoffmethode. Int Rev Ge-
Dollard estuary and its consequences for the growth of samten Hydrobiol 53:601–633
phytoplankton and microphytobenthos. Neth J Sea Res Hübel H, Wolff C, Meyer-Reil LA (1998) Salinity, inorganic
15:196–216 nutrients, and primary production in a shallow coastal
Colijn F, de Jonge VN (1984) Primary production of micro- inlet in the Southern Baltic Sea (Nordrügenschen Bodden)
phytobenthos in the Ems-Dollard estuary. Mar Ecol Prog Results from long-term observations (1960–1989). Int Rev
Ser 14:185–196 Gesamten Hydrobiol 83:479–499
Colijn F, Van Buurt G (1975) Influence of light and tempera- Jassby AD, Platt T (1976) Mathematical formulation of the
ture on the photosynthetic rate of marine benthic diatoms. relationship between photosynthesis and light for phyto-
Mar Biol 31:209–214 plankton. Limnol Oceanogr 21:155–168
Correns M, Jäger F (1979) Beiträge zur Hydrographie der Jørgensen BB, des Marais DJ (1990) The diffusive boundary
Nordrügenschen Bodden. I. Einführung in das Unter- layer of sediments: oxygen microgradients over a micro-
suchungsgebiet. Wasserstandsverhältnisse und Wasser- bial mat. Limnol Oceanogr 35:1343–1355
haushalt. Acta Hydrophys 24:149–177 Jørgensen BB, Revsbech NP (1985) Diffusive boundary layers
Correns M, Jäger F (1982) Beiträge zur Hydrographie der and the oxygen uptake of sediments and detritus. Limnol
Nordrügenschen Bodden. II. Strömungsverhältnisse, Salz- Oceanogr 30:111–122
und Sauerstoffhaushalt. Acta Hydrophys 27:5–22 Karsten U, Kühl M (1996) Die Mikrobenmatte — das kleinste
de Brouwer JFC, De Deckere EMGT, Stal LJ (2003) Distribu- Ökosystem der Welt. Biol Unserer Zeit 26:16–26
tion of extracellular carbohydrates in three intertidal mud- Kohl JG, Nicklisch A (1988) Ökophysiologie der Algen.
flats in Western Europe. Estuar Coast Shelf Sci 56:313–324 Gustav Fischer, Jena
Epping EHG (1996) Benthic phototrophic communities and Koop K, Boynton WR, Wulff F, Carman R (1990) Sediment-
the sediment-water exchange of oxygen, Mn(II), Fe(II), water oxygen and nutrient exchanges along a depth
and silicic acid. PhD dissertation, Rijksuniversiteit Gro- gradient in the Baltic Sea. Mar Ecol Prog Ser 63:65–77
ningen Krause H (1977) Produktionsbiologisch-ökologische Unter-
Falkowski PG, Raven JA (1997) Aquatic photosynthesis. suchungen am Mikrophytobenthos im Zingster Strom der
Blackwell Science, Oxford Darß-Zingster Boddenkette (südliche Ostsee). MS thesis,
Gargas E (1972) Measurements of microalgal primary produc- Universität Rostock
tion (phytoplankton and microbenthos) in the Smalands- Kühl M, Lassen C, Jørgensen BB (1994) Light penetration and
havet (Denmark). Ophelia 10:75–89 light intensity in sandy marine sediments measured with
Garstecki T, Güber A, Premke K, Verhoeven R, Arndt H, Wick- irradiance and scalar irradiance fibre-optic microprobes.
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 197
Mar Ecol Prog Ser 105:139–148 Ecol Prog Ser 76:81–89
Lange-Bertalot H (1998) A first ecological evaluation of the Pickney J, Zingmark RG (1993) Biomass and production of
diatom flora in Central Europe, species diversity, selective benthic microalgal communities in estuarine habitats.
human interactions and the need of habitat protection. Estuaries 16:887–897
Oceanol Stud 2:5–12 Plante-Cuny MR, Bodoy A (1987) Biomasse et production pri-
Lassen C, Ploug H, Jørgensen BB (1992) A fibre-optic scalar maire du phytoplancton et du microphytobenthos de deux
irradiance microsensor: application for spectral light mea- biotopes sableux (Golfe de Fos, France). Oceanol Acta 10:
surements in sediments. FEMS Microbiol Ecol 86:247–254 223–237
Li Y, Gregory S (1974) Diffusion of ions in sea water and Radach G, Berg J, Hagmeier E (1990) Long-term changes of
in deep-sea sediments. Geochim Cosmochim Acta 38: the annual cycles of meteorological, hydrographic, nutri-
703–714 ent and phytoplankton time-series at Helgoland and at
Lozán JL, Kausch H (1998) Angewandte Statistik für Natur- LV Elbe 1 in the German Bight. Cont Shelf Res 10:305–328
wissenschaftler. Parey, Berlin Raine RCT (1983) The effect of nitrogen supply on the photo-
MacIntyre HL, Cullen JJ (1996) Primary production by sus- synthetic quotient of natural phytoplankton assemblages.
pended and benthic microalgae in a turbid estuary: time- Bot Mar 26:417–423
scales of variability in San Antonio Bay, Texas. Mar Ecol Rasmussen H, Jørgensen BB (1992) Microelectrode studies of
Prog Ser 145:245–268 seasonal oxygen uptake in a coastal sediment: role of
MacIntyre HL, Geider RJ, Miller DC (1996) Microphyto- molecular diffusion. Mar Ecol Prog Ser 81:289–303
benthos: the ecological role of the ‘Secret Garden’ of un- Revsbech NP, Jørgensen BB (1983) Photosynthesis of benthic
vegetated, shallow-water marine habitats. I. Distribution, microflora measured with high spatial resolution by the
abundance and primary production. Estuaries 19:186–201 oxygen microprofile method: capabilities and limitations
Meyercordt J, Meyer-Reil LA (1999) Primary production of of the method. Limnol Oceanogr 28:749–756
benthic microalgae in two shallow coastal lagoons of dif- Revsbech NP, Jørgensen BB (1986) Microelectrodes: their use
ferent trophic status in the southern Baltic Sea. Mar Ecol in microbial ecology. Adv Microb Ecol 9:293–353
Prog Ser 178:179–191 Revsbech NP, Jørgensen BB, Brix O (1981) Primary pro-
Meyercordt J, Gerbersdorf S, Meyer-Reil LA (1999) Signifi- duction of microalgae in sediments measured by oxygen
cance of pelagic and benthic primary production in two microprofile, H14CO3-fixation, and oxygen exchange
shallow coastal lagoons of different degrees of eutrophica- methods. Limnol Oceanogr 26:717–730
tion in the southern Baltic Sea. Aquat Microb Ecol 20: Revsbech NP, Jørgensen BB, Blackburn TH, Cohen Y (1983)
273–284 Microelectrode studies of the photosynthesis and O2,
Meyer-Reil LA (1994) Microbial life in sedimenatry biofilms — H2S and pH profiles of a microbial mat. Limnol Oceanogr
the challenge to microbial ecologists. Mar Ecol Prog Ser 28:1062–1074
112:303–311 Rieling T (1999) Remineralisation organischen Materials in
Meyer-Reil LA, Neudörfer F (1998) Structure and function of Boddengewässern Mecklenburg-Vorpommerns unter be-
photoheterotrophic biofilms along a gradient of eutrophi- sonderer Berücksichtigung der Bedeutung von Partikeln
cation in a coastal inlet of the southern Baltic Sea. Pro- und Aggregaten. PhD dissertation, Universität Greifswald
ceedings of the Workshop on the 4th and 5th December Rieling T, Gerbersdorf S, Stodian I, Black HJ, Dahlke S,
1997 at the UFZ Centre for Environmental Research Köster M, Meyercordt J, Meyer-Reil LA (2000) Benthic
Leipzig-Halle. In: Becker PM (ed) Microbiology of microbial decomposition of organic matter and nutrient
polluted aquatic ecosystems. UFZ-Bericht 10, Leipzig, fluxes at the sediment –water interface in a shallow coastal
p 199–200 inlet of the southern Baltic Sea (Nordrügensche Bodden).
Miller DC, Geider RJ, MacIntyre HL (1996) Microphyto- In: Flemming BW, Delafontaine MT, Liebezeit G (eds)
benthos: the ecological role of the ‘Secret Garden’ of Muddy coast dynamics and resource management. Proc
unvegetated, shallow-water marine habitats. II. Role in Mar Sci Vol 2. Elsevier Science BV, Amsterdam,
sediment stability and shallow-water food webs. Estuaries p 175–184
19:202–212 Rizzo WM (1990) Nutrient exchange between the water
Mills DK, Wilkinson M (1986) Photosynthesis and light in column and a subtidal benthic microalgal community.
estuarine benthic microalgae. Bot Mar 29:125–129 Estuaries 13:219–226
Neudörfer F, Meyer-Reil LA (1998) Kleinräumige Bestim- Rizzo WM, Lackey GJ, Christian RR (1992) Significance of
mung respiratorischer und photosynthetischer Prozesse euphotic, subtidal sediments to oxygen and nutrient
mit Sauerstoffmikroelektroden in Sedimenten. In: Ver- cycling in a temperate estuary. Mar Ecol Prog Ser 86:51–61
einigung für Allgemeine und Angewandte Mikrobiologie Robinson DH, Arrigo KR, Iturriaga R, Sullivan CW (1995)
(VAAM) (eds) Mikrobiologische Charakterisierung aqua- Microalgal light-harvesting in extreme low-light environ-
tischer Sedimente, Methodensammlung. Oldenbourg ments in McMurdo Sound, Antarctica. J Phycol 31:508–520
Verlag, Wien, p 245–260 Sakshaug E, Bricaud A, Dandonneau Y, Falkowski PG and
Nielsen LP, Christensen PB, Revsbech NP, Sørensen J (1990) 5 others (1997) Parameters of photosynthesis: definitions,
Denitrification and photosynthesis in stream sediment theory and interpretation of results. J Plankton Res 19:
studied with microsensor and whole-core techniques. 1637–1670
Limnol Oceanogr 35:1135–1144 Schiewer U (1998) 30 years’ eutrophication in shallow
Oren A, Kühl M, Karsten U (1995) An endoevaporitic micro- brackish waters — lessons to be learned. Hydrobiologia
bial mat within a gypsum crust: zonation of phototrophs, 363:73–79
photopigments, and light penetration. Mar Ecol Prog Ser Schlungbaum G, Baudler H, Nausch G (1994) Die Darss-Zing-
51:151–159 ster Boddenkette — ein typisches Flachwasserästuar an
Pankow H (1990) Ostsee-Algenflora. VEB Gustav Fischer, der südlichen Ostseeküste. Rostock Meeresbiol Beitr 2:
Jena 5–26
Pickney J, Zingmark RG (1991) Effects of tidal stage and sun Schnese W (1973) Untersuchungen zur Produktionsbiologie
angles on intertidal benthic microalgal productivity. Mar des Greifswalder Boddens (südliche Ostsee). I. Die Hydro-
198 Aquat Microb Ecol 41: 181–198, 2005
graphie: Salzgehalt, Sauerstoffgehalt, Temperatur und shore marine sediments. Limnol Oceanogr 27:552–556
Sestongehalt. Wiss Z Univ Rostock Math-Naturwiss Reihe Underwood GJC, Boulcott M, Raines CA, Waldron K (2004)
22:629–639 Environmental effects on exopolymer production by
Schubert H, Sagert S, Forster RM (2001) Evaluation of the marine benthic diatoms: dynamics, changes in composi-
different levels of variability in the underwater light field tion, and pathways of production. J Phycol 40:293–304
of a shallow estuary. Helgoländer Wiss Meeresunters 55: Walsby AE (1997) Numerical integration of phytoplankton
12–22 photosynthesis through time and depth in a water column.
Shaffer GP, Onuf CP (1983) An analysis of factors influencing New Phytol 136:189–209
the primary production of the benthic microflora in a Wasmund N (1986) Ecology and bioproduction in the micro-
southern California lagoon. Neth J Sea Res 17:126–144 phytobenthos of the chain of shallow inlets (Boddens)
Sommer U (1994) Planktologie. Springer-Verlag, Berlin south of the Darss-Zingst Peninsula (Southern Baltic Sea).
Sommer U (1998) Biologische Meereskunde. Springer-Verlag, Int Rev Gesamten Hydrobiol 71:153–178
Berlin Wasmund N (1990) Characteristics of phytoplankton in
Stodian I, Gerbersdorf S, Rieling T, Black HJ, Köster M, Meyer- brackish waters of different trophic levels. Limnologica 20:
Reil LA (2000) Geochemical investigations of iron and man- 47–51
ganese in coastal sediments of the southern Baltic Sea. In: Wasmund N, Kell V (1991) Characterization of brackish
Flemming BW, Delafontaine MT, Liebezeit G (eds) Muddy coastal waters of different trophic levels by means of
coasts dynamics and resource management. Proc Mar Sci, phytoplankton biomass and primary production. Int Rev
Vol 2. Elsevier Science BV, Amsterdam, p 149–160 Gesamten Hydrobiol 76:361–370
Sundbäck K, Snoeijs P (1991) Effects of nutrient enrichment Wasmund N, Schiewer U (1994) Überblick zur Ökologie und
on microalgal community composition in a coastal shal- Produktionsbiologie des Phytoplanktons der Darß-Zing-
low-water sediment system: an experimental study. Bot ster Boddenkette (südliche Ostsee). Rostock Meeresbiol
Mar 34:341–358 Beitr 2:41–60
Sundbäck K, Enoksson V, Granéli W, Pettersson K (1991) Webb WL, Newton M, Starr D (1974) Carbon dioxide ex-
Influence of sublittoral microphytobenthos on the oxygen change of Alnus rubra: a mathematical model. Oecologia
and nutrient flux between sediment and water: a labora- 17:281–291
tory continuous-flow study. Mar Ecol Prog Ser 74:263–279 Whitney DE, Darley WM (1983) Effect of light intensity upon
Täuscher L (1976) Ökologische Untersuchungen am Mikro- salt marsh benthic microalgal photosynthesis. Mar Biol 75:
phytobenthos im Zingster Strom der Darß-Zingster 249–252
Boddenkette (südliche Ostsee). MS thesis, Universität Wiltshire KH (1992) The influence of microphytobenthos on
Rostock oxygen and nutrient fluxes between eulittoral sediments
Teubner J (1989) Quantitative und qualitative Erfassung sub- and associated water phases in the Elbe Estuary. In:
merser Makrophyten 1986/87— Luftbildanalysen. MS Colombo G, Ferrari I, Ceccherelli VU, Rossi R (eds) Proc
thesis, Universität Rostock 25th Eur Mar Biol Symp. Olsen & Olsen, Fredensborg,
Ullman WJ, Aller RC (1982) Diffusion coefficients in near- p 63–70
Editorial responsibility: Kevin Carman, Submitted: January 16, 2004; Accepted: August 7, 2005
Baton Rouge, Louisiana, USA Proofs received from author(s): November 4, 2005
Vol. 41: 181–198, 2005 Published November 25
Aquat Microb Ecol
Microphytobenthic primary production in the
Bodden estuaries, southern Baltic Sea, at two
study sites differing in trophic status
Sabine Ulrike Gerbersdorf 1, 2,*, Jürgen Meyercordt 1, Lutz-Arend Meyer-Reil1
1
Institut für Ökologie, Ernst-Moritz-Arndt-Universität Greifswald, Schwedenhagen 6, 18565 Kloster/Hiddensee, Germany
2
Present address: Institut für Wasserbau, Versuchsanstalt, Pfaffenwaldring 61, Universität Stuttgart, 70550 Stuttgart, Germany
ABSTRACT: Eutrophication in coastal areas has stimulated phytoplankton growth, sustaining a high
biomass and leading to a shift in the underwater light field. With the significance of the microphyto-
benthos for oxygen supply and carbon budget of both benthic and pelagic habitats in mind, the pos-
sible effects of reduced light availability were investigated in the estuarine Bodden area (southern
Baltic Sea) at 2 sites differing in trophic status — the eutrophic Kirr Bucht (KB) and the mesotrophic
Rassower Strom (RS). Using for the first time microsensors in Bodden sediments, it was possible to
visualize small-scale heterogeneity in the light regime, photosynthetic activity and oxygen penetration
with high spatial and temporal resolution. Hence, differences at the 2 sites related to sediment charac-
teristics (KB sandy, RS muddy), and photoautotrophic biomass (benthic chlorophyll a in the upper
1 cm, µg cm– 3 = 11 to 48 at KB and 13 to 17 at RS) could be ruled out. Calculations of benthic primary
production based solely on microelectrode measurements revealed substantial oxygen fluxes and car-
bon fixation rates at in situ light intensities at both study sites (e.g. gross primary production, GPP, mg
C m–2 h–1 = 28 to 80 at KB and 3 to 36 at RS). The different combinations of water transparency (pelagic
chlorophyll a, µg l–1 = 12 to 33 at KB and 1.3 to 4.5 at RS), light attenuation k (3.17 m–1 at KB, 0.61 m–1
at RS) and water depth (0.6 m at KB, 3.4 m at RA) have led to a similar light availability for benthic
algae on the sediment surface at both study sites. Consequently, the benthic algae had comparable
productivity at both sites, with maximum primary production, P Bmax (mg C mg–1 chlorophyll a h–1) of
0.29 to 1.46 at KB and 0.17 to 1.63 at RS; and were adapted to rather low light conditions, with light
saturation, Ek (µE m–2 s–1) of 22 to 152 at KB and 10 to 116 at RS). Varying with season, microphytoben-
thic photosynthetic activity accounted for 26 to 59 and 2 to 53% to the total primary production at the
KB and RS, respectively, with the highest contribution in spring coincident with the most favourable
light conditions at the sediment surface. With an annual average of about 37 and 30% (KB and RS, re-
spectively), the contribution of the microphytobenthos to total production was significant and compa-
rable at both study sites. Nevertheless, the higher trophic status at KB resulted in a change in the ben-
thic microalgal community towards sedimentated phytoplankton species and had a negative impact
on microphytobenthic primary production rates. This was estimated by calculating the gross primary
production for varying water depths on the basis of the different water transparency at the 2 sites.
KEY WORDS: Microphytobenthos · Primary production · Microsensors · Microprofiles · Phytoplankton ·
Benthic–pelagic coupling · Estuary · Baltic Sea
Resale or republication not permitted without written consent of the publisher
INTRODUCTION phytobenthos is presumed to be important in stabilis-
ing sediments (de Brouwer et al. 2003) and in con-
In shallow non-tidal waters, the light climate allows trolling nutrient fluxes directly at the sediment/water
the development of a photoautotrophic benthic com- interface through nutrient uptake (Sundbäck et al.
munity (Wasmund 1986, Miller et al. 1996). The micro- 1991, Rizzo et al. 1992, Wiltshire 1992). Moreover,
*Email: sabine.gerbersdorf@iws.uni-stuttgart.de © Inter-Research 2005 · www.int-res.com
182 Aquat Microb Ecol 41: 181–198, 2005
oxygenation of the sediment surface layers by photo- tat and its role as an important link in benthic–pelagic
synthetic activity leads to indirect geochemical fixation coupling after resuspension events (Gerbersdorf et al.
of nutrients and heavy metals (Koop et al. 1990, 2004).
Nielsen et al. 1990). Furthermore, the supply of oxygen Herein, we report the first comprehensive investiga-
through photosynthetic activity determines the occur- tions on microphytobenthos over a seasonal range to
rence of heterotrophic organisms such as protozoans be carried out in the Bodden estuaries at 2 study sites
and meiofauna in the upper sediment (Berninger & differing in trophic status. In contrast to recent pub-
Epstein 1995). In terms of primary production, the lications (Meyercordt & Meyer-Reil 1999, Meyercordt
microphytobenthic community may account for the et al. 1999), microphytobenthic primary production
main part of carbon fixation, especially in shallow rates in the present study were determined solely by
waters (Cadee & Hegeman 1974, Plante-Cuny & Bodoy microelectrodes. Moreover, interpolation of the data
1987, MacIntyre & Cullen 1996, MacIntyre et al. 1996, for the time intervals between measurements was
Underwood et al. 2004). done using the Walsby (1997) model. Especially in the
During the last few decades, phytoplankton growth low light range, microelectrode measurements are far
has been stimulated in many coastal zones by an in- more sensitive than other integrative methods, and
creased supply of nutrients, which sustains a high bio- allow the direct determination of gross photosynthesis
mass and has led to a shift in the underwater light rates within the sediment (Revsbech et al. 1981, Revs-
climate (Radach et al. 1990, Schiewer 1998). Several bech & Jørgensen 1983, Sommer 1994, Karsten & Kühl
publications have dealt with the pelagic primary pro- 1996, Gerbersdorf 2000). Thus, the measurements of
duction in the Bodden estuaries (estuarine areas in benthic production rates are more reliable, and hence
the Southern Baltic Sea, hereafter referred to as ‘the calculations on the sediment oxygen budget and car-
Bodden’) (Hübel 1968, Börner & Kell 1982). These pub- bon supply to the benthic habitat as well as to the
lications have clearly documented increased phyto- pelagic habitat after resuspension are more precise.
plankton biomass and primary production rates related Moreover, microprofiles of light and oxygen reveal
to change in the trophic status over the last 30 yr mutual changes in abiotic factors and the resulting
(Wasmund 1990, Wasmund & Schiewer 1994, Bachor microphytobenthic photosynthetic activity at high spa-
et al. 1996, Hübel et al. 1998). Increased phytoplankton tial and temporal resolution, which can only be
abundance has led to a reduction in light penetration detected as a sum otherwise (Revsbech & Jørgensen
and hence a decline in macrophytes and submerged 1986, Lassen et al. 1992). The Walsby (1997) model
flowering plants (Behrens 1982, Teubner 1989). The takes the reflection characteristics of the light at the
change in the underwater light climate may also signif- water surface under different solar angles into consid-
icantly affect the microphytobenthic primary produc- eration. Hence the calculations of the underwater light
tion, as light intensity is considered to be the primary field and corresponding production rates (especially
factor controlling benthic photosynthesis (Colijn 1982, with regard to the different trophic status of the 2 study
Pickney & Zingmark 1993). Despite the significance of sites) achieved further precision in the present study.
the microphytobenthos, comparatively little data has Possible physiological adaptations of the benthic algae
been published on microphytobenthic primary produc- to prevailing light conditions were examined using
tion and the possible effects of eutrophication, globally photosynthesis/irradiance (P /E) curves with data on
and for the sublittoral in particular. For the Bodden, maximum photosynthetic capacity (Pmax), photosyn-
only a few studies have focused on the microphyto- thetic efficiency (α) and the light saturation coefficent
benthic community and primary production rates (Ek) (Kohl & Nicklisch 1988, Pickney & Zingmark 1991,
(Täuscher 1976, Krause 1977, Wasmund 1986). To Falkowski & Raven 1997, Barranguet et al. 1998).
date, almost nothing has been recorded on the present To examine possible effects of eutrophication on the
status of microphytobenthos in the Bodden in general benthic microalgal community (Sundbäck & Snoeijs
and the possible effects of light limitation on microphy- 1991), the species composition of the phytoplankton
tobenthic production and community dynamics in par- and microphytobenthos was determined microscopi-
ticular. Only recently has data on the primary produc- cally at the 2 study sites.
tion rates of benthic microalgae and their contribution
to the total primary production of the shallow Bodden
as a function of trophic status been reported (Gerbers- MATERIALS AND METHODS
dorf & Meyercordt 1999, Gerbersdorf et al. 2000). The
photoautotrophic character of the flocculent sediment Study sites. Two study sites in the estuarine Bodden
surface layer, its fractions and its aggregates indicated area, southern Baltic Sea (Fig. 1) differing in morpho-
the significance of the microphytobenthos in the Bod- metry, hydrography and trophic status, were investi-
den for the oxygen/carbon budget of the benthic habi- gated at different seasons. The Kirr-Bucht (KB) is an
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 183
Sampling and treatment. Sampling took
place once each season (July 1996, Sep-
tember/October 1996, January 1997, April
1997) at each study site. For benthic pri-
mary production measurements, undis-
turbed sediment cores of about 100 mm
length and 1.1 l of overlying ambient water
were taken using cylindrical Plexiglas
tubes (length 300 mm, internal diameter
100 mm) either with a hand-manipulated
coring device or with a multicorer device
(Barnett et al. 1984) at Sites KB and RS,
respectively (the device used depended
on the shallowness of the investigation
area). The sediment cores were carefully
transported to the laboratory and placed in
a room protected from electrical ‘noise’.
Sediment cores were placed into a water
bath and the in situ temperature was
kept constant by a cooling system. During
photosynthesis measurements, the sedi-
ment cores were illuminated under differ-
Fig. 1. Study sites. A: Kirr Bucht (inner part of the Darss-Zingster Boddenkette);
B: Rassower Strom (outer part of the Nordrügensche Boddenkette), both located ent light intensities by a halogen cold light
in the estuarine Bodden area of the southern Baltic Sea. DK: Denmark source (Schott, KL 1500 electronic), with
the lamp at a 45° angle to avoid shading
by the microsensor. The exposure of the
inner area in the Darss-Zingster Boddenkette, charac- samples to different irradiances (ranging from in situ to
terised by low salinities (5.0 to 6.6) and high nutrient artificial high light intensities) was alternated by dark
concentrations (Gerbersdorf et al. 2004, S. Dahlke pers. periods. The water column above the sediment was
comm.). Its high chlorophyll a concentrations (12 to aerated to keep the oxygen concentration constant. To
33 µg l–1) and pelagic primary production rates (Hübel measure pelagic primary production and respiration,
et al. 1998) are typical for eutrophic waters (Wasmund water samples were incubated in situ in 3 sets of 4
& Kell 1991). In a water depth of 0.6 m, the sediment is transparent and 4 black bottles over a period of about
sandy with an organic carbon content of 1%. Rassower 10 h. Each set of bottles was exposed at a different
Strom (RS) is one of the outer Bodden estuaries of the water depth (below surface, above bottom and mid
Nord-Rügensche Boddenkette, and consequently is water; for further details see Meyercordt et al. 1999).
more strongly influenced by the Baltic Sea, having Natural light intensities at sediment surface. Nat-
higher salinities (8.2 to 9.4) and low nutrient concentra- ural in situ light intensities experienced by the micro-
tions (Gerbersdorf et al. 2004, S. Dahlke pers. comm.). phytobenthos were calculated for each season for both
Because of its lower chlorophyll a concentrations (1.3 to sites (Table 1). The light attenuation coefficient (k) in
4.5 µg l–1) and pelagic primary production rates (Hübel the water column was calculated from vertical light
et al. 1998), this study site is regarded as mesotrophic intensity profiles in decimetre to metre steps by a
(Wasmund & Kell 1991). The sediment in approxi- spherical underwater sensor (LI-COR LI 193SA). In
mately 4 m water depth consists of sandy mud with an combination with data on photosynthetically active
organic carbon content of up to 4% on its surface. In radiation (PAR, 400 to 700 nm), which was continu-
January 1997, the RS was not accessible due to ice ously measured above the water surface (LI-COR LI
cover. Therefore, another nearby sampling station, the 190SA), k values were used to calculate the lowest,
Klosterloch, which is comparable to the RS in terms of medium and highest irradiances at the sediment
water and sediment characteristics, was used for this surface for the relevant periods (Table 1).
month. (For simplicity, the term ‘Rassower Strom, RS’, Chlorophyll a and phaeopigment a. Pigments in
will be used hereafter for data from Klosterloch and water samples of a defined volume were concentrated
RS.) More details on the morphology and hydrography on Whatman GF/C filters, which were immediately
of KB and RS are available in Correns & Jäger (1979, deep-frozen. The sediment cores were sectioned into
1982), Schlungbaum et al. (1994), Meyercordt et al. different layers at intervals of 1 cm and each layer was
(1999) and Gerbersdorf et al. (2004). mixed thoroughly to avoid patchiness in the pigment
184 Aquat Microb Ecol 41: 181–198, 2005
Table 1. Light attenuation k (m–1) in the water column and and the light sensors were modified after Lassen et al.
range of in situ light intensities (lowest to highest) available to (1992). The precise position of the microsensors was ob-
the microphytobenthos at the sediment surface in the Kirr
served through a dissection microscope, using a micro-
Bucht and Rassower Strom (Bodden area of the southern
Baltic Sea). Irradiance calculated on an hourly basis from manipulator with a control unit (Märzhäuser & Wetz-
constantly measured photosynthetically active radiation lar, Type DC 3-K right and MS314) for positioning.
above the water surface and light attenuation in the water The microsensors determine oxygen gradients at
column, averaged for relevant month the sediment/water interface, caused by photosyn-
thetic and heterotrophic activity, under dark and light
Month k Light intensity (µE m–2 s–1)
conditions. The resulting oxygen fluxes (upwards out
Low Medium High
of the sediment into the water column and downwards
Kirr Bucht into deeper sediment horizons) have been used to cal-
July 1996 3.48 75 180 300 culate oxygen consumption/production (Revsbech et
October 1996 3.31 26 153 222
January 1997 2.17 10 141 197 al. 1981, Sommer 1994). For these calculations, the dif-
April 1997 3.73 18 198 168 fusion coefficient of oxygen in the water and sediments
Rassower Strom as well as the porosity of the sediment must be taken
July 1996 0.57 45 117 180 into account (Li & Gregory 1974, Ullmann & Aller 1982,
October 1996 0.73 12 180 120
January 1997 0.56 20 135 100 Revsbech & Jørgensen 1986, Rasmussen & Jørgensen
April 1997 0.59 19 107 177 1992). Oxygen microelectrodes can also be used to
directly determine gross photosynthesis by the light/
dark shift method (Revsbech et al. 1981, Revsbech &
concentrations. From each sediment layer, 5 subsam- Jørgensen 1983, 1986). Thereby a steady state of
ples of 0.5 cm3 each were taken with a cut-off syringe oxygen distribution will be achieved under constant
and stored deep frozen in centrifuge tubes. Pigment conditions and the initial decrease in oxygen within
analysis following the guidelines of the Helsinki Com- 1 s after darkening the sediment reflects gross photo-
mission (HELCOM 1988). Pigments were extracted in synthesis (Revsbech & Jørgensen 1983, Karsten & Kühl
96% ethanol followed by spectrophotometric readings 1996). This is the only method that takes into account
at 665 nm before and after acidification with HCl to variation in oxygen consumption in darkness and at
correct for the phaeopigment a concentrations (Perkin- different irradiances arising from differential expan-
Elmer UV/VIS spectrometer lambda 2). sion of the oxic layer and/or changes in volumetric
Light and oxygen fluxes. On the assumption that respiration rates in response to oxygen supply (Epping
oxygenic photosynthesis is the main pathway of car- 1996). To avoid changes in oxygen concentration due
bon dioxide fixation in the Bodden, changes in oxygen to osmotic effects, the vertical spatial resolution of the
concentrations were recorded in the water samples light/dark shift method is restricted to layers of approx-
and sediment to calculate pelagic and benthic photo- imately 100 µm by the oxygen diffusion velocity, which
synthesis, respectively. The terms photosynthesis and is 67 µm s–1 according to the Einstein-Smoluchowski
primary production are interchangeable in the law (Neudörfer & Meyer-Reil 1998).
following text. Microscale variations in the occurrence of benthic
Oxygen exchange: Since oxygen fluxes can be organisms and their metabolic activities are well docu-
derived from microelectrode profiles only in sedi- mented (Revsbech et al. 1983, Jørgensen & Revsbech
ments, the pelagic primary production and respiration 1985, review by Meyer-Reil 1994) and may hamper the
was measured in situ by changes in the oxygen con- extrapolation of rates measured by microelectrodes.
centration in water samples under light and dark con- Therefore, to obtain a representative overview of res-
ditions, determined by the Winkler method. The light piration and photosynthetic activity in the sediments, 6
conditions for the incubated water samples were to 12 vertical profiles were taken randomly from the
recorded via a spherical underwater sensor (LI-COR LI sediment surface of each sediment core.
193SA; for further details see Meyercordt et al. 1999.) Primary production. Pelagic gross photosynthesis
Microelectrode measurements: Microsensors were was calculated as the sum of respiration and net photo-
used to determine the light intensity, light attenuation synthesis. Microphytobenthic photosynthetic activity
and the photic zone (zPAR), as well as the oxygen con- was determined similarly, but also directly by the
centration and penetration depth (zoxygen) in the upper light/dark shift method, whereby the gross photosyn-
sediment layers in relation to illumination at the sedi- thesis rates for the different sediment layers were
ment surface. The microsensors enabled measurements related to volume and multiplied by the vertical expan-
of high vertical (50 to 100 µm) and temporal (< 0.1 s) sion (zphot) of the measured profile of photosynthetic
resolution. The Clark-type oxygen microelectrodes activity (Revsbech et al. 1981, Revsbech & Jørgensen
were built according to Revsbech & Jørgensen (1986) 1983, 1986).
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 185
Gross primary production rates were expressed as body, but also the reflection characteristics of the water
C-equivalents using the conversion factor 1.2 (Mills surface. Therefore, calculations of light availability for
& Wilkinson 1986) and taking main substrates and phytoplankton in different water depths as well as for
products of dioxide fixation into account (Burris 1981, microphytobenthos at the sediment surface gained fur-
Raine 1983, Sakshaug et al. 1997). Gross primary pro- ther precision. Using these light field calculations,
duction rates of pelagic and microphytobenthic area pelagic primary production was calculated in 0.1 m
were normalised to chlorophyll a concentrations in the steps from the water surface down to the bottom, and
water samples and in the flocculent sediment surface integrated over the whole water column on an hourly
layer, respectively, to correct for algal biomass. The basis. Benthic primary production and respiration
different resolution of sediment pigment profiles were also calculated on an hourly basis using the
(0.5 cm steps in the upper layers) and oxygen/gross calculated PAR values at the sediment surface.
photosynthesis microprofiles (100 µm) did not allow Statistics. The assumptions of normality and homo-
appropriate algal biomass correction, and represents a geneity of variance were tested using visual assess-
challenge for further experiments. ment of the frequency histogram and normal plot, as
Photosynthesis models. In a literature overview, well as skewness and kurtosis, both of which provide
Jassby & Platt (1976) discussed different photosynthe- information on the symmetry and peakiness of a dis-
sis models that have been used to mathematically tribution (Armitage & Berry 1994). Additionally, the
describe oxygen production rates as a function of light Shapiro-Wilk W-test indicated normal distribution of
conditions (photosynthesis vs. irradiance, P/E, curves). the data (‘Analyse-it’ for Microsoft Excel). Hence, a
We tested 4 models to describe the experimental data: 2-way ANOVA was applied to test for differences
between the means of samples classified by the cate-
P B = Pmax αE /(Pmax + αE) Baly (1935)
gories of 2 factors (study site and season) (‘Analyse-it’
P B = Pmax tanh (αE /Pmax) Jassby & Platt (1976)
for Microsoft Excel). The model tested for the main
P B = Pmax [1 – exp (– αE /Pmax )] Webb et al. (1974)
effects of study site and season, as well as interactions
P B = Pmax [1 – exp (– αE /Pmax)] Walsby (1997)
between study site and season. When significant (p <
+ (E β) + R
0.05) effects were detected, an a posteriori comparison
where P B represents production rate at a given illumi- were made using Tukey’s test (‘Analyse-it’ for Micro-
nation, E; Pmax is maximum gross primary production soft Excel; Armitage & Berry 1994, Lozán & Kausch
rate under optimal light conditions (= photosynthetic 1998).
capacity); α is photosynthetic efficiency in the light-
limited part of the P/E curve; the Pmax:α ratio yields Ek,
which is an indicator of photosynthetic adaptation to RESULTS
prevailing light conditions; β is photoinhibition under
high light intensities; and R is respiration. Normalised Species composition
to chlorophyll a concentrations, the terms P Bmax and αB
will be used forthwith instead of the area-related terms For the eutrophic Kirr Bucht (KB), microscopic stud-
Pmax and α. ies revealed a phytoplankton community typical for
Adaptation of the models to the experimental data inner Bodden estuaries, with high diversity and little
was estimated by differences in the data obtained from seasonal variation. The following were the most com-
the fitted curve. The total error (sum of squared differ- monly found species (Pankow 1990, Lange-Bertalot
ences between the measured data and the fitted curve) 1998): Aphanocapsa sp., Aphanothece clathrata, Gom-
depends strongly on the absolute values of the photo- phosphaeria lacustris, G. pusilla, Merismopedia glauca,
synthetic rates. Thus, the total error was divided by the M. punctata, Microcystis aeruginosa and M. botrys
sum of the gross primary production rates of the fitted (Cyanophyceae: Chroococcales); Anabaena torulosa,
curve. In this way, the degree of adaptation of the dif- A. spiroides, Lyngbya contorta and Oscillatoria tenuis
ferent models to the experimental data was obtained (Cyanophyceae: Nostocales); Skeletonema costatum
for the different seasons and both study sites (data not (Bacillariophyceae: Centrales); Diatoma vulgare and
shown). The photosynthesis model of Webb et al. Surirella ovalis (Bacillariophyceae: Pennales); Botryo-
(1974) best described the experimental data. coccus braunii, Kirchneriella lunaris, Monoraphidium
Modelling. An interpolation of the data for times contortum, Oocystis pelagica, Pediastrum boryanum,
between experiments was achieved by applying P/E Scenedesmus sp. (7 species) and Tetrastrum triangu-
parameters and measured respiration rates to the lare (Chlorophyceae: Chlorococcales).
photosynthesis model of Walsby (1997) with the aid of In contrast, the phytoplankton community at the
constantly measured PAR data. Walsby’s (1997) model mesotrophic study site Rassower Strom (RS) resembled
considers not only PAR attenuation within the water the species composition of the offshore region (Arkona-
186 Aquat Microb Ecol 41: 181–198, 2005
see), with seasonal successions from diatom blooms in Cocconeis scutellum, C. placentula, Cymbella affinis,
spring to Cyanobacteria dominance in summer and Diploneis didyma, D. smithii, Epithemia turgida,
Dinophyceae development in autumn. The following Fragilaria sp., Navicula pygmaea, N. digitoradiata,
species were most abundant (Pankow 1990, Lange- Nitzschia compressa, N. constricta, Opephora sp.,
Bertalot 1998): Anabaena torulosa and Oscillatoria Pleurosigma sp., Surirella ovata). Thus, the species
tenuis (Cyanophyceae: Nostocales); Cyclotella comta, composition in the RS sediments differed clearly from
Chaetoceros danicus, Coscinodiscus radiatus, Melosira that in the water column.
sp., Skeletonema costatum and Stephanodiscus sp.
(Bacillariophyceae: Centrales); Gyrosigma sp., Pleuro-
sigma sp. and Surirella sp. (Bacillariophyceae: Pen- Pigment concentrations (chlorophyll a:phaeopigment a)
nales); Dinophysis sp., Gymnodinium sp., Peridinium
granii, Prorocentrum minimum and P. balticum (Dino- In the sediments of both study sites, highest chloro-
phyceae); Oocystis sp. and Pediastrum boryanum phyll a concentrations occurred mainly within the first
(Chlorophyceae: Chlorococcales). sediment horizon of 1 cm depth (seasonal range of 13
In the KB, Cyanobacteria (Chroococcales) and to 48 µg cm– 3 and 13 to 17 µg cm– 3 at KB and RS,
Chlorophyceae (Chlorococcales) dominated the algal respectively), and decreased with increasing sediment
community both on and within the sediment and in the depth (Fig. 2). In KB sediments, chlorophyll a concen-
water column, from where most species originated. trations were up to 9 times higher than the phaeopig-
Benthic pennate diatom species were found in low ment concentrations. In contrast, in the sediments at
abundances (Amphora sp., Cocconeis sp., Navicula RS, concentrations of active and degraded pigments
sp., Nitzschia sp., Surirella sp.). At the RS, a true micro- were similar. Sediments at KB contained up to 3 times
phytobenthos was established, with a high diversity of higher chlorophyll a concentrations than the sediments
pennate diatoms: Achnanthes delicatula, Amphora sp., at RS (Fig. 2).
0 S 0 S
-1 -1
-2 -2
-3 -3
Depth (cm)
-4 -4
-5 -5 Chl a RS
Phaeo a RS
-6 -6 Chl a KB
-7 -7 Phaeo a KB
-8 -8
-9 -9
A B
-10 -10
0 10 20 30 40 50 0 10 20 30 40 50
0 S 0 S
-1 -1
-2 -2
-3 -3
Depth (cm)
-4 -4
-5 -5
-6 -6
-7 -7
-8 -8
-9 -9
C D
-10 -10
0 10 20 30 40 50 0 10 20 30 40 50
Pigment concentration (µg cm-3) Pigment concentration (µg cm-3)
Fig. 2. Vertical profiles of chlorophyll a (chl a) and phaeopigment a (phaeo a) concentrations in sediments of Kirr Bucht (KB) and
Rassower Strom (RS) in (A) summer 1996, (B) autumn 1996, (C) winter 1997 and (D) spring 1997. Pigment detection began
in the flocculent layer on top of the sediment surface (S, ) and continued downwards to a depth of 10 cm
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 187
Photic zone (zPAR) intensities at the sediment surface, the peaks of photo-
synthetic activity moved downwards in the sediment.
According to the definition of the euphotic zone in In the sediments of RS, the highest gross production
the pelagic environment (Sommer 1998), the photic rates were always just beneath the sediment surface,
zone is defined as the sediment depth at which PAR e.g. zphot, spring, 0.8 mm RS; Fig. 4B), even with
is reduced to 1% of incident irradiance. Light inten- increasing incident irradiance (data not shown). The
sity and light penetration were measured using extension of the photosynthetic active zone as well as
spherical glass-fibre microsensors in the upper sedi- the gross primary production rates were significantly
ment horizons, which were exposed to various irra- higher in KB sediments than in RS sediments (p <
diances (Fig. 3). A clear light intensity peak was 0.0001; Table 2).
detected just below (Fig. 3A) and at (Fig. 3B) the
sediment surface; the peak was most pronounced at
higher light intensities. With increasing surface irra- Aerobic zone (zoxygen)
diance, the light penetrated significantly into deeper
sediment layers to a maximum depth beyond which In correlation with increasing incident irradiance,
increases in incident irradiances did not result in fur- the enhanced activity of photoautotrophic organisms
ther extension of the photic zone (Fig. 3). In the sandy led to higher oxygen production rates and an
sediments of KB, the photic zone was always more extended oxic layer in the upper sediment layers
pronounced than in the muddy sediments of RS (p < (Fig. 5). zoxygen is defined as the sediment depth at
0.0001, Table 2, Fig. 3). which 1 µmol l–1 of oxygen concentration is de-
Table 2. Mean ± SD (n = 3 to 10) oxygen consumption (O2consum: mmol O2 m–1 h–1)
Photosynthetic zone (zphot ) under dark conditions and extension (µm) of aerobic zone (zoxygen) under dark and
medium light conditions, and extension of photic layer (zPAR) and photosynthetic
Increasing irradiance at the sedi- active layer (zphot) under medium in situ light intensities in sediments of both study
sites at different seasons. nd: not determined
ment surface leading to deeper light
penetration into the sediment could
Date O2consum zoxygen zPAR zphot
activate photoautotrophic organisms Dark Dark Medium light Medium light Medium light
in deeper layers. Nevertheless, the
zone of photosynthetic activity did Kirr Bucht
not extend to the full extent of the 1 Jul 1996 –0.97 ± 0.24 1300 ± 400 1700 ± 150 2000 ± 150 800 ± 170
7 Oct 1996 –0.66 ± 0.19 1800 ± 150 3200 ± 150 3000 ± 400 1100 ± 300
photic zone (Table 2, Fig. 4). In 27 Jan 1997 –0.60 ± 0.08 2500 ± 150 6100 ± 210 1900 ± 000 nd
the sandy sediments of the KB, a 7 Apr 1997 .–120 ± 0.27 2400 ± 290 4700 ± 200 3200 ± 200 1600 ± 600
zone with pronounced photosynthetic Rassower Strom
activity was detected (e.g. spring, 8 Jul 1996 –0.89 ± 0.16 1600 ± 200 3500 ± 110 1800 ± 000 570 ± 60
1.6 mm), with several peaks of maxi- 30 Sep 1996 –0.79 ± 0.15 2300 ± 230 2600 ± 500 1600 ± 100 0100 ± 300
mal oxygen production in deeper 15 Jan 1997 –0.39 ± 0.06 3050 ± 230 2800 ± 250 1300 ± 000 nd
14 Apr 1997 –0.72 ± 0.15 3400 ± 220 6700 ± 140 1500 ± 150 0700 ± 100
layers (Fig. 4A). With increasing light
A 2 B 2
1 1
Depth (mm)
0
0
-1 1200
-1 900
1200 600
900 300
-2 600
300 -2 220
100
150
-3
60 -2 -1
-3
10
µE m s 60 µE m-2 s-1
-4 -4
0 200 400 600 800 1000 1200 1400 0 200 400 600 800 1000 1200 1400
PAR (µE m-2 s-1) PAR (µE m-2 s-1)
Fig. 3. Vertical light profiles in sediments of the (A) Kirr Bucht and (B) Rassower Strom, determined by a glass-fibre optical sensor
at different illumination intensities in autumn 1996. Horizontal line at depth zero marks the sediment surface, with the negative
values indicating sediment depth. PAR: photosynthetically active radiation
188 Aquat Microb Ecol 41: 181–198, 2005
2
GPP (nmol O2 cm-3 s-1) A
A 0 0.5 1.0 1.5 2.0 2.5 3.0 75
1 150
0 Surface 350
Depth (mm)
0
-0.4
-1
Depth (mm)
-0.8
-2 600
-1.2 900
-3 1200
2400 µE m2 s-1
-1.6
-4
0 200 400 600 800 1000 1200
-2.0
0 200 400 600 800 1000 1200 1400
O2-concentration (µmol l-1)
0 20 40 60 80 100 120 140 2
PAR (µE m-2 s-1)
B 75
150
1 350
Depth (mm)
GPP (nmol O2 cm-3 s-1) 0
0 0.5 1.0 1.5 2.0 2.5 3.0
B
0 -1
Surface
600
-2
-0.4 900
-3 1200
Depth (mm)
-0.8 µE m2 s-1
2400
-4
-1.2 0 100 200 300 400
O2 concentration (µmol l-1)
-1.6 Fig. 5. Vertical oxygen profiles in sediments of the (A) Kirr
Bucht and (B) Rassower Strom, determined by the oxygen
-2.0 Clark-type microelectrode under different illumination inten-
0 200 400 600 800 1000 1200 1400 sities in autumn 1996. Further details as for Fig 3
O2-concentration (µmol l-1)
0 20 40 60 80 100 120 140
PAR (µE m-2 s-1)
Oxygen consumption and net primary production
Fig. 4. Gross primary production, GPP (bars), oxygen concen-
trations and PAR at different sediment depths at medium
in situ light intensity in spring 1997 at (A) Kirr Bucht and At both study sites, oxygen consumption and net
(B) Rassower Strom primary production within the sediments (determined
under dark and light conditions, respectively) showed
a clear seasonal trend, with lowest rates in winter
tectable. According to this definition, oxygen micro- (Table 2, Fig. 6). Oxygen consumption and net primary
profiles indicated an extension of the aerobic zone of production rates within the sandy KB sediments were
1.3 to 2.5 mm and 1.6 to 3.4 mm (seasonal range; both significantly higher than in the muddy RS sedi-
Table 2) in dark conditions in the sediments of the ments (p < 0.0001; Table 2, Fig. 6). Nevertheless, the
KB and RS, respectively (differences between the ratios of gross oxygen production:oxygen consump-
study sites were significant at the level p < 0.0003). tion, representing photoautotrophic and heterotrophic
Even under illumination, the extension of zoxygen was processes (omitting for the latter the chemical oxygen
still higher in the RS sediments than in the KB sedi- demand in the sediment), were much higher in KB
ments in spring and summer (p < 0.0001; Table 2). than RS, and most pronounced under the highest natu-
Nevertheless, the higher benthic microalgal biomass rally occurring light intensities (seasonal range: KB,
and photosynthetic rates at KB resulted in up to 6 5 to 10; RS, 0.8 to 4). Nevertheless, the oxygen pro-
times higher maxima of oxygen concentrations in the duction in the RS sediments was sufficient to meet the
upper sediment layers of KB compared to RS (p < oxygen demand even at low light intensities (except in
0.0001; Figs. 4 & 5). winter), as indicated by the positive oxygen net fluxes.
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 189
0.7 A 2.0
A
0.6
GPP (mg C mg-1 chl a h-1)
1.5
0.5
NPP (µmol O2 cm-2 h-1)
0.4
1.0
0.3
July 1996, r = 0.84
0.5
0.2 October 1996, r = 0.99
April 1997, r = 0.96
0.1 January 1997, r = 0.98
0
0 500 1000 1500 2000 2500
0.0
–0.1 B 2.0
0.7
B
GPP (mg C mg-1 chl a h-1)
1.5
0.6
0.5
NPP (µmol O2 cm-2 h-1)
1.0
0.4
July 1996, r = 0.84
0.3 0.5
October 1996, r = 0.99
April 1997, r = 0.96
0.2 January 1997, r = 0.98
0
0.1 0 500 1000 1500 2000 2500
PAR (µE m-2 s-1)
0.0
Fig. 7. Seasonal photosynthesis/irradiance (P/E) curves for
microphytobenthos in (A) Kirr Bucht and (B) Rassower Strom
–0.1
L M H L M H L M H L M H sediments calculated according to the model of Webb et
Jul 1996 Sep 1996 Jan 1997 Apr 1997 al. (1974)
Fig. 6. Mean (± SD) net primary production (NPP) of micro-
phytobenthos in sediments of the (A) Kirr Bucht and (B) Ras-
both sites, the maximal primary production rates fol-
sower Strom, at different in situ light intensities (L: low;
M: medium; H: high) in different seasons lowed seasonal changes in temperature (r = 0.82 and
0.71) and mean light intensities (r = 0.85 and 0.76) (KB
and RS, respectively). The α B values, reflecting photo-
Gross primary production synthetic efficiency, showed negative correlations with
The areal gross primary production rates were sig- Table 3. Parameters of photosynthesis/irradiance (P/E)
nificantly higher at KB than RS (p = 0.0282). Nor- curves; data normalised to chlorophyll a (chl a), showing
photosynthetic efficiency, αB (mg C mg–1 chl a) h–1 (µE m–2
malised to chlorophyll a, the gross primary produc- s–1)–1, maximum photosynthetic capacity, P Bmax (mg C mg–1
tion rates were still slightly higher in winter in the chl a h–1), and light saturation, Ek (µE m–2 s–1) related to
KB sediments than in the RS sediments, but were microphytobenthic primary production for both study sites
comparable in summer at the 2 sites (Fig. 7). In in different seasons
autumn 1996 and spring 1997, the specific produc-
tion rates were significantly higher in the sediments Kirr Bucht Month Rassower Strom
αB P Bmax Ek αB P Bmax Ek
of RS (p < 0.0001).
The P Bmax values, reflecting photosynthetic capacity 0.0096 1.46 152 Jul 1996 0.0133 1.54 116
under prevailing light conditions, showed a clear sea- 0.0123 0.66 54 Sep/Oct 1996 0.0121 1.28 106
sonal trend in KB sediments, but the trend was less 0.0131 0.29 22 Jan 1997 0.0171 0.17 10
0.0124 0.40 32 Apr 1997 0.0189 1.63 86
pronounced for RS (Table 3, Fig. 7). Nevertheless, at
190 Aquat Microb Ecol 41: 181–198, 2005
temperature (r = 0.75 and 0.82) and mean light condi- Contribution of benthic primary production
tions (r = 0.81 and 0.76) (KB and RS, respectively).
Thus, light saturation Ek , defined as the ratio P Bmax:α B, Since net oxygen production and respiration rates
correlated with both temperature (r = 0.77 and 0.93) can be derived from oxygen microprofiles for sediments
and mean light intensity (r = 0.82 and 0.94) (KB and RS, only, pelagic primary production was determined by
respectively). the oxygen exchange method. The interpolation of the
measured benthic and pelagic primary production rates
over 24 h for those days on which measurements were
The benthic habitat — sink or source of oxygen? made showed that the microphytobenthos contributed
from 26 to 59% and 2 to 53% to the total primary pro-
On the basis of the foregoing (R, α B, P Bmax), and duction at KB and RS, respectively. The relative contri-
linked with respiration rates and the results of con- bution of benthic primary production was highest in
stant PAR measurements, the model of Walsby (1997) spring at both sites. A further interpolation of the mea-
allowed interpolation of the net primary production sured data with constantly determined PAR values and
rates for the time intervals between measurements. the Walsby (1997) model over the course of 1 yr showed
This was initially performed for the 24 h of each sam- that, as an annual average, the microphytobenthos ac-
pling day in the different seasons. Whereas for the 8 h counted for 37 and 30% of the total primary production
illumination a positive oxygen flux was calculated at KB and RS, respectively (Fig. 9). The carbon fixation
even in the low light range at both study sites (except rates by the microphytobenthos were calculated as 2 to
in winter at RS: Fig. 6), daily calculation of the oxygen 17 g C m–2 mo–1 (113 g C m–2 yr–1) for KB (Fig. 9A) and
budget indicated negative oxygen fluxes in summer 0.2 to 7 g C m–2 mo–1 (42 g C m–2 yr–1) for RS (Fig. 9B).
and autumn for RS and in winter for KB (Fig. 8). For The pelagic gross production rates, integrated over the
both study sites, integrated over 24 h, the highest pos- water depth, were 2 times higher in the shallow KB (5 to
itive oxygen fluxes for the benthic habitat were calcu- 30 g C m–2 mo–1, 190 g C m–2 yr–1) than in the deeper RS
lated for spring. (2 to 24 g C m–2 mo–1, 108 g C m–2 yr–1) (Fig. 9).
5 5
KB + 14.1 mmol O2 m-2 d-1
4
A KB + 5.4 mmol O2 m-2 d-1
4
B RS – 10.3 mmol O2 m-2 d-1
NPP (mmol O2 m-2 h-1)
RS – 8.6 mmol O2 m-2 d-1
3 3
2 2
1 1
0 0
–1 –1
–2 –2
0 2 4 6 8 10 12 14 16 18 20 22 24 0 2 4 6 8 10 12 14 16 18 20 22 24
5 5
C KB + 0.8 mmol O2 m-2 d-1
D
NPP (mmol O2 m-2 h-1)
4 RS – 11.7 mmol O2 m-2 d-1 4
3 3
2 2
1 1
0 0
–1 –1 KB + 20.6 mmol O2 m-2 d-1
RS – 2.7 mmol O2 m-2 d-1
–2 –2
0 2 4 6 8 10 12 14 16 18 20 22 24 0 2 4 6 8 10 12 14 16 18 20 22 24
Time (h-1) Time (h-1)
Fig. 8. Benthic net primary production (NPP), interpolated using Walsby’s model (1997), over the days on which sampling was
carried out (see Table 2) in Kirr Bucht and Rassower Strom sediments in different seasons. (A) summer 1996; (B) autumn 1996;
(C) winter 1997; (D) spring 1997
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 191
30 100 Microphytobenthos: light climate and
A species composition
25
80
In recent decades, the nutrient load of
20 municipal, agriculture and industrial water
60 has led to an increase in phytoplankton bio-
15 mass in the Bodden (Wasmund & Schiewer
40
1994, Schiewer 1998), resulting in drastic
10 changes in the underwater light field.
Phytoplankton adds significantly to the
% of MPB on total GPP
20 scattering and absorption of light in the
GPP (mg C m-2 mo-1)
5
water column reducing light intensity and
0 0 altering the spectral composition (Schubert
et al. 2001, S. U. Gerbersdorf unpubl.).
Thus, water transparency at the eutrophic
30 100
study site, Kirr Bucht, was 4 to 6 times lower
B than at the mesotrophic study site, Ras-
25
80 sower Strom. Nevertheless, at the sediment
surface, light availability (the main abiotic
20 factor influencing microphytobenthic pho-
60
tosynthesis) was similar in both areas due to
15 different morphologies and water depths
40 (KB, 0.6 m; RS, 3.4 m). However, the species
10 composition of the benthic algae differed
qualitatively at the 2 sites. Microscopic
20
5 investigation revealed that Cyanobacteria
of the order Chroococcales and Chloro-
0 0 phyceae of the order Chlorococcales were
ry ry h ril y e y st r r r r
nua brua Marc Ap Ma Jun Jul ugu mbe tobe mbe mbe dominant on the sediment surface of KB;
Ja Fe A pte Oc ove ece
Se N D with a similar composition of species (e.g.
Fig. 9. Carbon fixation rates (gross primary production, GPP) for the Gomphospheria lacustris, Merismopedia
benthal (black bars) and the pelagial (grey bars), interpolated using the punctata, Scenedesmus quadricauda and
Walsby model (1997) on a monthly basis, in the (A) Kirr Bucht and Oocystis sp.) in the water column. Only a
(B) Rassower Strom. Curve indicates contribution of photosynthetic few benthic diatoms such as Gyrosigma
activity of the microphytobenthos (MPB) to total GPP
balticum and Surirella sp. were present in
KB sediments, indicating that most of the
‘microphytobenthos’ originated from the
DISCUSSION overlying water column. In contrast, the species
composition in the sediment and water column clearly
The significance of microphytobenthic primary differed at RS. The microphytobenthos at RS mainly
production for the aquatic habitat is obvious (Koop et consisted of pennate diatoms such as Navicula sp. and
al. 1990, Rizzo 1990, Wiltshire 1992, Berninger & Amphora sp. However, in terms of oxygen and carbon
Epstein 1995, MacIntyre & Cullen 1996, MacIntyre et supply, the sedimented pelagic algae in the KB are
al. 1996, de Brouwer et al. 2003). Nevertheless, only comparable to an actual microphytobenthos; thus, we
some 100 papers in the last few decades have exam- have used the term ‘microphytobenthos’ for both study
ined the subject of microphytobenthos on a global sites.
scale, and even fewer have investigated the sublit-
toral zone. Until recently (Meyercordt et al. 1999,
Gerbersdorf 2000, Gerbersdorf et al. 2004), almost no Highly resolved measurements in the sediment
investigations on the microphytobenthos had been
carried out in the Bodden areas of the southern Microelectrode studies are mainly known from the
Baltic Sea. The present study examined microphyto- intertidal zone (e.g. Barranguet et al. 1998) or within
benthic primary production in 2 Bodden areas differ- microbial mats (e.g. Oren et al. 1995) and the investi-
ing in trophic status, and thus in conditions for the gations presented here are the first to use micro-
microphytobenthos. sensors in the Bodden estuaries. The microsensors
192 Aquat Microb Ecol 41: 181–198, 2005
provided very detailed information on the spatial and oxygen penetration not only under dark conditions,
temporal heterogeneity of light, photosynthetic activ- but also under illumination in spring and summer.
ity and oxygen within the sediment itself. The sedi- The question remains as to whether the higher oxygen
ments at both study sites had different soil charac- supply in KB sediments leads to enhanced microbial
teristics, which altered the light climate within the processes, as indicated by the relatively high ratio of
sediment in predictable ways. The photic zone (zPAR) active and degraded pigments, or whether a greater
in the sandy sediments of KB was about twice as deep supply of fresh organic material through primary pro-
(seasonal range 1.4 to 3.2 mm) as that in the muddy duction may have led to the higher oxygen consump-
sediments of RS (seasonal range 0.9 to 2.0 mm) under tion rates in the KB sediments. More important is
in situ light intensities. This was in agreement with the opportunity (now provided by microsensors) to
the findings of Jørgensen & des Marais (1990) and examine the varying penetration of zoxygen in seasonal
Kühl et al. (1994), who determined a photic zone of terms and its consequences in the sediments of both
1.3 to 4.6 and 0.2 to 2.0 mm for sandy and muddy sed- study sites.
iments, respectively. Light attenuation is determined
mainly by absorption, which is stronger in sediments
with higher organic content. If absorption is low, Significance of microphytobenthos
strong scattering can retain a high light intensity at a
given depth; this is especially enhanced near optical The occurrence of many organisms is determined by
boundaries, resulting in maximum scalar irradiance. the aerobic conditions within the sediment. Thus, the
This was seen within the first 1 mm of the strongly highest abundance and vertical distribution of meio-
scattering, sandy sediment of KB, leading to peaks in fauna (Arlt & Georgi 1999), heterotrophic flagellates
light intensity of up to 140% relative to incident light and amoebae (Garstecki et al. 1999) as well as bacteria
from above (up to 200% in sandy sediments in- (Rieling 1999) (determined simultaneously in parallel
vestigated by Kühl et al. 1994 and Oren et al. 1995). investigations) matched the expansion of the aerobic
In contrast, in RS sediments, pronounced light inten- zone at both study sites. In anoxic layers, sulphate-
sity peaks occurred directly at the sediment surface reducing bacteria became dominant in the sediments
due to scattering and reflection. In agreement with lit- of both study sites (Babenzien & Voigt 1999). Further-
erature data, the light attenuation coefficient for the more, the importance of the aerobic layer to redox
first 5 mm sediment layer was much lower in the conditions and nutrient fluxes was shown by the
sandy sediments of KB than in the muddy sediments release of manganese and iron (Stodian et al. 2000)
of RS (seasonal k range of 0.4 to 1.0 mm–1 and 1.3 to and the release of o-phosphate and ammonia (Rieling
2.0 mm–1, respectively). et al. 2000) under anoxic conditions, whereas these
Under in situ irradiances, the photosynthetic active compounds are bound to the sediment in oxidised
zone (zphot) ranged down to a maximum of 2 mm form. The microphytobenthos also assimilates nutrients
depth in KB sediments, but to a maximum depth of for photosynthetic activity, thereby reducing the
only 1 mm in RS sediments, as measured by the nutrient fluxes of o-phosphate and ammonia under
light/dark shift method. Consequently, zphot did not illumination significantly (Gerbersdorf et al. 2000, Riel-
resemble zPAR at either study site. Presumably, less ing et al. 2000).
than 20 µE m–2 s–1 was not sufficient to support the Initiated by illumination, migration towards the sur-
photosynthetic activity of the pelagic species in the face and photosynthetic activity of the algae lead to
KB sediments. At the same time, the pennate diatoms stabilisation of the sediment along with mat formation
in RS sediments could migrate to upper layers with and EPS (extracellular polymeric substances) produc-
better light availability. Despite a generally more tion/excretion (S. U. Gerbersdorf unpubl.). This is im-
extensive zPAR in KB sediments, zphot at this site was portant in shallow waters, where even low winds can
significantly more pronounced only in spring com- otherwise lead to resuspension events (Schnese 1973).
pared to RS. Nevertheless, at KB, 3 times higher pig- With regard to the benthic–pelagic coupling, micro-
ment concentrations in the upper 0.5 cm (up to 50 µg benthic algae can contribute not only to the oxygen
cm– 3) resulted in significantly higher rates of photo- and carbon supply within the sediment, but also to that
synthetic activity and up to 6 times higher oxygen in the water column through resuspension processes
concentrations in the upper layers compared to RS (Schiewer 1998). Therefore, in addition to investigating
(maximum of 1100 and 300 µmol l–1, respectively). the spatial and temporal heterogeneity of the meta-
This did not necessarily lead to a higher oxygen pen- bolic processes within the sediment itself, we exam-
etration in KB sediments, as the oxygen consumption ined the primary production of the microphytobenthos
there was generally higher than in RS sediments. as one of the main driving forces in the carbon budget
Consequently, the muddy RS sediments had higher of these shallow waters.
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 193
Primary production of microphytobenthos Physiological adaptations of microphytobenthos
The high benthic chlorophyll a concentrations in Over the course of the year, photosynthetic rates var-
the KB sediments reflected the high biomass of ied not only as a function of biomass, but also (strongly)
phytoplankton at this eutrophic site, which was as a function of abiotic factors (temperature, r = 0.82
deposited on the sediment surface. Under in situ and 0.71; light, r = 0.85 and 0.76, for KB and RS, respec-
light conditions, the benthic gross primary produc- tively), in accordance with reports in the literature (e.g.
tion rates in KB sediments (28 to 80 mg C m–2 h–1) Blanchard & Guarini 1996). Temperature affects the
were 3 times higher than in RS. Thus, benthic pri- specific activities of enzymes (Epping 1996), which in
mary production rates in KB sediments were well turn affect C-assimilation as well as the electron trans-
within the range of data for highly productive diatom port chain (Kohl & Nicklisch 1988). Light intensity
associations in the Wadden Sea. Colijn & de Jonge determines photosynthetic capacity by influencing the
(1984) and Barranguet et al. (1998) determined orientation, size and number of reaction centres and
benthic gross production rates of 10 to 115 mg C m–2 the capacity of the Calvin cycle (Kohl & Nicklisch
h–1 and 11 to 58 mg C m–2 h–1 in the tidal zone, 1988). Since temperature and light were comparable at
respectively, depending on season. Moreover, the the sediment surface of both study sites, no significant
photosynthetic rates in KB sediments at light intensi- differences in the physiological adaptations of the 2
ties up to 350 µE m–2 s–1 were 1.5 times higher than algal communities would be expected. Nevertheless,
in biofilms along an eutrophication gradient in Bod- the parameters of the P/E curves such as photosyn-
den waters (34.4 to 94.5 mg C m–2 h–1 at radiation thetic capacity (Pmax), photosynthetic efficiency (α) and
levels of 100 to 800 µE m–2 s–1, Meyer-Reil & Neu- light saturation (Ek), should indicate general adapta-
dörfer 1998). In contrast, RS sediments had primary tions of the benthic algae to, for example, low light
production rates (3 to 36 mg C m–2 h–1) that were regimes when data from both study sites are compared
comparable with data obtained for deeper sublittoral with data in the literature (Kohl & Nicklisch 1988,
coastal areas. Gargas (1972) and Herndl et al. (1989) Pickney & Zingmark 1991, Falkowski & Raven 1997,
determined gross primary production rates of 0.5 to Barranguet et al. 1998).
21 mg C m–2 h–1 at 4 m depth and 10 to 13 mg C m–2 Normalised for chlorophyll a, the P Bmax, maximum
h–1 at 7 to 22 m depth, respectively. Nevertheless, photosynthetic values were (except for winter) lower
the microphytobenthos at RS displayed as much as for KB benthic microalgae than for those at RS, although
half of the photosynthetic activity measured in the medium light availability at the sediment surface
biofilms in Bodden waters (Meyer-Reil & Neudörfer was comparable or even higher at KB. This could indi-
1998), although biofilms are usually known as sys- cate nutrient limitation at times of high photosynthetic
tems with high metabolic activities. activities in the sediment, as described by Sundbäck
In regard to a possible decline in the microphyto- & Snoeijs (1991), although usually nutrient limitation
benthos due to eutrophication, excessive phyto- in the benthic habitat is less likely because benthic
plankton development and decreasing light avail- microalgae can assimilate nutrients directly out of the
ability at the sediment surface, comparison of our interstitial water (Shaffer & Onuf 1983). Also, the high
data with earlier findings at the 2 study sites would benthic algal biomass in the upper layers of the KB
have been of particular interest. Unfortunately, no sediments could have shaded the algae in deeper
data for RS and only a few earlier publications for KB layers, resulting in lower mean photosynthetic capac-
are available for microphytobenthic primary produc- ity rates integrated over the depths measured. Mac-
tion. Wasmund (1986) measured benthic primary Intyre & Cullen (1996) demonstrated higher P Bmax val-
production in a similar range to our data (7 to ues in the upper than the lower sediment depths (6 to
117 mg C m–2 h–1), but the sediments he investigated 10 compared to 0.6 to 2.8 mg C mg–1 chl a h–1) as a
originated from a depth of only 15 to 20 cm, which is result of adaptation to different light conditions. The
much less than the water depth at our study site. It is P Bmax values in the present paper were in the range of
not feasible to discuss the decline in microphyto- 0.17 to 1.63 mg C mg–1 chl a h–1 at both study sites and
benthos using the few data currently available, thus comparable to data from other sublittoral offshore
especially considering the well-known variations in regions. Plante-Cuny & Bodoy (1987) determined P Bmax
primary production rates that can occur within a few of 0.46 to 1.23 mg C mg–1 chl a h–1 in sandy sediments
hours even at the same investigation point (Blan- at 0.5 m depth in the Golfe de Fos, France. In the
chard et al. 2001). Monitoring programmes are Wadden Sea, the algae experience temporally higher
strongly recommended to reveal possible effects of light intensities and temperature, resulting in higher
eutrophication on the microphytobenthos on a long- chlorophyll-specific production rates. Thus, Pickney &
term basis. Zingmark (1991) reported variation in P Bmax between
194 Aquat Microb Ecol 41: 181–198, 2005
0.27 and 4.42 mg C mg–1 chl a h–1, with highest values sen for our measurements to be representative for both
at low tide. Barranguet et al. (1998) measured photo- locations. Accordingly, the KB sediments could be a
synthetic capacity of up to 13 mg C mg–1 chl a h–1 in source of oxygen except in wintertime, and the RS sed-
tidal areas of the Dutch Wadden Sea. iments mainly a sink of oxygen except from late spring
Together with the αB values, which indicate the to summer.
photosynthetic efficiency of photon utilisation, the
photosynthetic capacity, P Bmax determines the light
saturation value Ek, an indicator for photosynthetic Contribution of microphytobenthos to total
acclimatisation to prevailing light conditions. In gen- primary production
eral, relatively low Ek is expected under low light
conditions, when benthic microalgae utilise the photon To estimate the significance of microphytobenthic
flux more efficiently (relatively high αB) and achieve primary production in relation to total primary produc-
maximal photosynthetic activity quite quickly (rela- tion, the pelagic primary production rates must be
tively low P Bmax). As for P Bmax, αB and Ek were corre- taken into consideration. Because microelectrodes can
lated with temperature and light conditions at both only be used in the sediment, the photosynthetic activ-
study sites over the course of the year (P Bmax and Ek ity of phytoplankton was determined by the oxygen
positively, αB negatively). The seasonal Ek values exchange method. Both methods are well-fitted to the
ranged from 22 to 152 µE m–2 s–1 and from 10 to 116 µE nature of the relevant samples (pelagic production–ex-
m–2 s–1 for KB and RS, respectively, and reflected adap- change method for oxygen development and detection
tations of the microalgae to rather low light conditions within the water, benthic production–microelectrodes
at both study sites. This agrees with data in the litera- method for oxygen development and detection within
ture, which cover a broad range of light saturation the sediment) and thus, little difference resulting from
values (e.g. Robinson et al. 1995, McMurdo Sound, methodology was expected between the data sets for
Antarctica: 1.3 to 4.5 µE m–2 s–1; Whitney & Darley pelagic and benthic primary production. For sediment
1983, sand bank in Georgia: 2044 µE m–2 s–1). The Ek samples, microelectrodes gave much more reliable
values in the present paper were comparable to values results on benthic primary production than more inte-
for the tidal zone during high tide reported by Colijn & grative methods such as oxygen exchange measure-
Van Buurt (1975), where the turbidity of the water ments. Microelectrodes measure photosynthetic activ-
column led to high light attenuation and mean Ek ity directly at the production spot within the sediment,
values of 165 µE m–2 s–1. and both upward and downward oxygen fluxes are
included (Revsbech et al. 1981). Hence, gross benthic
primary production rates calculated on a monthly basis
The benthic habitat — sink or source of oxygen? in the present paper (KB: 2 to 17 g C m–2 mo–1; RS: 0.2
to 7 g C m–2 mo–1) were on average 2 times higher than
Under medium to maximum in situ light intensities, those reported by Meyercordt & Meyer-Reil (1999),
maximum photosynthetic capacity of the microphyto- who used the oxygen exchange method. The differ-
benthos was achieved at all seasons and at both study ences in benthic primary production rates determined
sites. The resulting photosynthetic oxygen production by both methods were more pronounced under the low
was able to meet the oxygen demand of the sediment, light regime, where oxygen production was at or
as indicated by positive oxygen fluxes at both study below the detection limit of the oxygen exchange
sites and at all seasons investigated, except in winter approach (Gerbersdorf 2000).
at RS. Nevertheless, the benthic microalgae only expe- Benthic and pelagic primary production rates were
rienced these irradiances during approximately 8 h of interpolated over the days on which sampling was
total illumination around noon on an annual average. carried out. On these days, the microphytobenthos
Applying the model of Walsby (1997), the data on oxy- accounted for about 26 to 59 and 2 to 53% of the total
gen consumption and production were interpolated primary production in KB and RS, respectively. The
over 24 h for the various sampling days (see Table 2) highest contribution (> 50%) to primary production by
using the determined respiration rates, P/E, and the the benthic algae was for spring, corresponding with
constantly measured PAR values. The daily oxygen the best light conditions at the sediment surface, while
budget of the benthic habitat (integrating dark and the lowest contribution (19 to 26%) was for summer
light periods) displayed negative oxygen fluxes for RS (except for winter at RS, where their contribution was
sediments in January, July and October and for KB exceptionally low), corresponding with low light avail-
sediments in January. Although photosynthetic activ- ability on that particular sampling day. In regard to the
ity and the light field are highly dynamic, interpolation high variability in the light field, the interpolation of
of the data on a monthly basis revealed the days cho- data on a monthly basis allowed more general con-
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 195
clusions as to the significance of microphytobenthic aries. The contribution of the benthic microalgae in
photosynthetic activities in the aquatic environment. terms of total primary production is substantial, and be-
Again, the lowest ratio of pelagic to benthic primary cause of the higher sensitivity of the detection method
production was for early spring, when the chlorophyll used (microelectrodes as opposed to the oxygen-
a concentrations in the water column indicated a 30% exchange method), even higher than that reported in
lower phytoplankton biomass resulting in a better light former publications. Taking into account the different
availability at the sediment surface compared to sum- water depths and water transparencies at the 2 study
mer and autumn. During the course of the year, the sites (eutrophic/mesotrophic status), the negative im-
contribution of the microphytobenthos to total primary pact of nutrient load and enhanced light attenua-
production was substantial and comparable at both tion caused by excessive phytoplankton development
study sites (37 and 30% for KB and RS, respectively). on microphytobenthic photosynthetic activity was re-
This can be explained by the morphology (water depth vealed. A true microphytobenthos was established at
at KB = 0.6 m, at RS = 3.4 m) and hydrography (light the mesotrophic study site, while pelagic algae species
attenuation at KB k = 3.17 m–1, at RS k = 0.61 m–1), at dominated on the sediment surface at the eutrophic
the 2 sites, which produced a similar light climate at site. A shift in benthic microalgal species composition
the sediment surface of both areas. Only by calculating could have serious consequences such as effects on
the benthic primary production for varying water productivity (different photon flux efficiencies) or sedi-
depths and taking into account the different water ment stability (differential EPS production). Although
transparency at each site could the effect of eutrophi- the input of sewage into rivers and coastal areas has
cation be revealed. been significantly reduced over the last few decades
(e.g. through the construction of numerous sewage
treatment plants), the internal load of nutrients within
Effects of trophic status the sediment (i.e. ‘legacy of the past’) remains a prob-
lem. Hence, monitoring programmes are still neces-
Because of the turbid and phytoplankton-rich water sary to assess the risks and evaluate possible effects of
column in the eutrophic KB, no light would be avail- eutrophication on the aquatic environment and enable
able at the sediment surface with a theoretical water development of appropriate remediation strategies in
depth of 3.4 m (the actual depth of the RS site), and endangered areas.
thus, no benthic photosynthetic activity would be pos-
sible there. In contrast, at the mesotrophic RS, signifi- Acknowledgements. The authors thank the crew of RV ‘Pro-
cant benthic primary production was measured at this fessor Fritz Gessner’ for assistance during sampling and Mar-
ion Köster, Ingrid Kreuzer, Frank Neudörfer, Georg Schubert,
water depth over the course of the year, except in win-
Joachim Timm and Wolfgang Zenke for excellent technical
ter. Based on a common depth of 0.6 m (the actual support. The authors are grateful to Helmut Hübel and
depth of the KB site), the benthic primary production Kirsten Wolfstein for enthusiastic teaching and help in the de-
rates would be similar at both study sites (Meyercordt termination of algal species. The investigations presented
& Meyer-Reil 1999), despite much less benthic micro- here were part of the joint research project ‘ÖKOBOD’ (Öko-
system Boddengewässer — Organismen und Stoffhaushalt) fi-
algal biomass at the RS. Assuming a common water nanced by the German BMBF (Bundesministerium für Bil-
depth of 2 m, resembling the mean water depth of the dung, Wissenschaft Forschung und Technologie).
Bodden, Meyercordt et al. (1999) showed that the
microphytobenthos would support 30 to 45% of the LITERATURE CITED
total primary production at RS, but only ≤0.3% at KB.
These calculations all support the hypothesis that Arlt G, Georgi F (1999) Meiofauna in der bentho–pelagischen
eutrophication coupled with excessive phytoplankton Kopplung. In: Black HJ, Köster M, Meyer-Reil LA (eds)
Ökosystem Boddengewässer — Organismen und Stoff-
development and decreasing light availability at the
haushalt (ÖKOBOD), BMBF. Abschlußbericht, Verbund-
sediment surface has strong negative impacts on projekt, Bodden 8. Institut für Ökologie der EMAU Greifs-
microphytobenthic primary production. wald, Kloster/Hiddensee, p 19–24
Armitage P, Berry G (1994) Statistical methods in medical
research. Blackwell Scientific, Oxford
Babenzien HD, Voigt A (1999) Bedeutung der Sulfatreduktion.
CONCLUSION In: Black HJ, Köster M, Meyer-Reil LA (eds) Ökosystem
Boddengewässer — Organismen und Stoffhaushalt (ÖKO-
The present study has shown the significance of the BOD), Abschlußbericht, Verbundprojekt, Bodden 8. Insti-
microphytobenthos for the oxygen supply and carbon tut für Ökologie der EMAU Greifswald, Kloster/Hidden-
see, p 67–72
budget of the benthic habitat (and, via resuspension,
Bachor A, von Weber M, Wiemer R (1996) Die Entwicklung
to the pelagic environment also), as evidenced by its der Wasserbeschaffenheit der Küstengewässer Mecklen-
primary production rates in the shallow Bodden estu- burg-Vorpommerns. Nährstoffeinträge aus Mecklenburg-
196 Aquat Microb Ecol 41: 181–198, 2005
Vorpommern in die Ostsee 1990–1995. Wasser Boden 48: ham SA (1999) Trophische Beziehungen innerhalb benthi-
26–36 scher mikrobieller Nahrungsgewebe. In: Black HJ, Köster
Baly ECC (1935) The kinetics of photosynthesis. Proc R Soc M, Meyer-Reil LA (eds) Ökosystem Boddengewässer — Or-
Lond Ser 117:218-239 ganismen und Stoffhaushalt (ÖKOBOD), Abschlußbericht,
Barnett PRO, Watson J, Connelly D (1984) A multiple corer for Verbundprojekt, Bodden 8. Institut für Ökologie der EMAU
taking virtually undisturbed samples from shelf, bathyal Greifswald, Kloster/Hiddensee, p 29–38
and abyssal sediments. Oceanol Acta 7:339–409 Gerbersdorf SU (2000) Die pelagische und mikrophytoben-
Barranguet C, Kromkamp J, Peene J (1998) Factors control- thische Primärproduktion in den Boddengewässern unter
ling primary production and photosynthetic characteris- Berücksichtigung der Sedimentauflage, ihrer Fraktionen
tics of intertidal microphytobenthos. Mar Ecol Prog Ser und Aggregate. PhD dissertation, Universität Greifswald
173:117–126 Gerbersdorf SU, Meyercordt J (1999) Primärproduzierende
Behrens J (1982) Soziologische und produktionsbiologische Prozesse in Pelagial und Benthal. In: Black HJ, Köster M,
Untersuchungen an submersen Pflanzengesellschaften Meyer-Reil LA (eds) Ökosystem Boddengewässer —
der Darß-Zingster Boddengewässer. PhD dissertation, Organismen und Stoffhaushalt (ÖKOBOD), Abschluß-
Universität Rostock bericht, Verbundprojekt, Bodden 8. Institut für Ökologie
Berninger UG, Epstein SS (1995) Vertical distribution of der EMAU Greifswald, Kloster/Hiddensee, p 39–47
benthic ciliates in response to the oxygen concentration Gerbersdorf SU, Black HJ, Meyercordt J, Meyer-Reil LA,
in an intertidal North Sea sediment. Aquat Microb Ecol Rieling T, Stodian I (2000) Significance of microphytoben-
9:229–236 thic primary production in the Bodden (southern Baltic
Blanchard GF, Guarini JM (1996) Studying the role of mud Sea). In: Flemming BW, Delafontaine MT, Liebezeit G
temperature on the hourly variation of the photosynthetic (eds) Muddy coasts dynamics and resource management.
capacity of microphytobenthos in intertidal areas. C R Proc Mar Sci, Vol 2. Elsevier Science BV, Amsterdam,
Acad Sci Sér III Sci Vie 319:1153–1158 p 127–136
Blanchard GF, Guarini JM, Orvain F, Sauriau PG (2001) Gerbersdorf SU, Meyercordt J, Meyer-Reil LA (2004) Micro-
Dynamic behaviour of benthic microalgal biomass in phytobenthic primary production within the flocculent
intertidal mudflats. J Exp Mar Biol Ecol 264:85–100 layer, its fractions and aggregates, studied in two shallow
Börner R, Kell V (1982) Einfluß von Nährstoffanreicherungen Baltic estuaries of different eutrophic status. J Exp Mar
auf die Biomasse, Artensequenz und Primärproduktion Biol Ecol 307:47–72
des Phytoplanktons während einer Komplexanalyse im HELCOM (Helsinki Commission) (1988) Guidelines for the
Zingster Strom (Juni 1981). Wiss Z Wilhelm-Pieck-Univ Baltic Monitoring Programme for the third stage. Loose
Rostock Math-Natwiss Reihe 31:53–56 sheet version of the Baltic Sea Environment Proceedings
Burris JE (1981) Effects of oxygen and inorganic carbon con- No. 27D. Helsinki Commission, Helsinki, p 1–60
centrations on the photosynthetic quotients of marine Herndl GJ, Peduzzi P, Fanuko N (1989) Benthic community
algae. Mar Biol 65:215–219 metabolism and microbial dynamics in the Gulf of Trieste
Cadée GC, Hegeman J (1974) Primary production of the ben- (Northern Adriatic Sea). Mar Ecol Prog Ser 53:169–178
thic microflora living on tidal flats in the Dutch Wadden Hübel H (1968) Die Bestimmung der Primärproduktion des
Sea. Neth J Sea Res 8:260–291 Phytoplanktons der Nordrügenschen Boddenkette unter
Colijn F (1982) Light absorption in the waters of the Ems- Verwendung der Radiokohlenstoffmethode. Int Rev Ge-
Dollard estuary and its consequences for the growth of samten Hydrobiol 53:601–633
phytoplankton and microphytobenthos. Neth J Sea Res Hübel H, Wolff C, Meyer-Reil LA (1998) Salinity, inorganic
15:196–216 nutrients, and primary production in a shallow coastal
Colijn F, de Jonge VN (1984) Primary production of micro- inlet in the Southern Baltic Sea (Nordrügenschen Bodden)
phytobenthos in the Ems-Dollard estuary. Mar Ecol Prog Results from long-term observations (1960–1989). Int Rev
Ser 14:185–196 Gesamten Hydrobiol 83:479–499
Colijn F, Van Buurt G (1975) Influence of light and tempera- Jassby AD, Platt T (1976) Mathematical formulation of the
ture on the photosynthetic rate of marine benthic diatoms. relationship between photosynthesis and light for phyto-
Mar Biol 31:209–214 plankton. Limnol Oceanogr 21:155–168
Correns M, Jäger F (1979) Beiträge zur Hydrographie der Jørgensen BB, des Marais DJ (1990) The diffusive boundary
Nordrügenschen Bodden. I. Einführung in das Unter- layer of sediments: oxygen microgradients over a micro-
suchungsgebiet. Wasserstandsverhältnisse und Wasser- bial mat. Limnol Oceanogr 35:1343–1355
haushalt. Acta Hydrophys 24:149–177 Jørgensen BB, Revsbech NP (1985) Diffusive boundary layers
Correns M, Jäger F (1982) Beiträge zur Hydrographie der and the oxygen uptake of sediments and detritus. Limnol
Nordrügenschen Bodden. II. Strömungsverhältnisse, Salz- Oceanogr 30:111–122
und Sauerstoffhaushalt. Acta Hydrophys 27:5–22 Karsten U, Kühl M (1996) Die Mikrobenmatte — das kleinste
de Brouwer JFC, De Deckere EMGT, Stal LJ (2003) Distribu- Ökosystem der Welt. Biol Unserer Zeit 26:16–26
tion of extracellular carbohydrates in three intertidal mud- Kohl JG, Nicklisch A (1988) Ökophysiologie der Algen.
flats in Western Europe. Estuar Coast Shelf Sci 56:313–324 Gustav Fischer, Jena
Epping EHG (1996) Benthic phototrophic communities and Koop K, Boynton WR, Wulff F, Carman R (1990) Sediment-
the sediment-water exchange of oxygen, Mn(II), Fe(II), water oxygen and nutrient exchanges along a depth
and silicic acid. PhD dissertation, Rijksuniversiteit Gro- gradient in the Baltic Sea. Mar Ecol Prog Ser 63:65–77
ningen Krause H (1977) Produktionsbiologisch-ökologische Unter-
Falkowski PG, Raven JA (1997) Aquatic photosynthesis. suchungen am Mikrophytobenthos im Zingster Strom der
Blackwell Science, Oxford Darß-Zingster Boddenkette (südliche Ostsee). MS thesis,
Gargas E (1972) Measurements of microalgal primary produc- Universität Rostock
tion (phytoplankton and microbenthos) in the Smalands- Kühl M, Lassen C, Jørgensen BB (1994) Light penetration and
havet (Denmark). Ophelia 10:75–89 light intensity in sandy marine sediments measured with
Garstecki T, Güber A, Premke K, Verhoeven R, Arndt H, Wick- irradiance and scalar irradiance fibre-optic microprobes.
Gerbersdorf et al.: Microphytobenthic primary production as a function of trophic status 197
Mar Ecol Prog Ser 105:139–148 Ecol Prog Ser 76:81–89
Lange-Bertalot H (1998) A first ecological evaluation of the Pickney J, Zingmark RG (1993) Biomass and production of
diatom flora in Central Europe, species diversity, selective benthic microalgal communities in estuarine habitats.
human interactions and the need of habitat protection. Estuaries 16:887–897
Oceanol Stud 2:5–12 Plante-Cuny MR, Bodoy A (1987) Biomasse et production pri-
Lassen C, Ploug H, Jørgensen BB (1992) A fibre-optic scalar maire du phytoplancton et du microphytobenthos de deux
irradiance microsensor: application for spectral light mea- biotopes sableux (Golfe de Fos, France). Oceanol Acta 10:
surements in sediments. FEMS Microbiol Ecol 86:247–254 223–237
Li Y, Gregory S (1974) Diffusion of ions in sea water and Radach G, Berg J, Hagmeier E (1990) Long-term changes of
in deep-sea sediments. Geochim Cosmochim Acta 38: the annual cycles of meteorological, hydrographic, nutri-
703–714 ent and phytoplankton time-series at Helgoland and at
Lozán JL, Kausch H (1998) Angewandte Statistik für Natur- LV Elbe 1 in the German Bight. Cont Shelf Res 10:305–328
wissenschaftler. Parey, Berlin Raine RCT (1983) The effect of nitrogen supply on the photo-
MacIntyre HL, Cullen JJ (1996) Primary production by sus- synthetic quotient of natural phytoplankton assemblages.
pended and benthic microalgae in a turbid estuary: time- Bot Mar 26:417–423
scales of variability in San Antonio Bay, Texas. Mar Ecol Rasmussen H, Jørgensen BB (1992) Microelectrode studies of
Prog Ser 145:245–268 seasonal oxygen uptake in a coastal sediment: role of
MacIntyre HL, Geider RJ, Miller DC (1996) Microphyto- molecular diffusion. Mar Ecol Prog Ser 81:289–303
benthos: the ecological role of the ‘Secret Garden’ of un- Revsbech NP, Jørgensen BB (1983) Photosynthesis of benthic
vegetated, shallow-water marine habitats. I. Distribution, microflora measured with high spatial resolution by the
abundance and primary production. Estuaries 19:186–201 oxygen microprofile method: capabilities and limitations
Meyercordt J, Meyer-Reil LA (1999) Primary production of of the method. Limnol Oceanogr 28:749–756
benthic microalgae in two shallow coastal lagoons of dif- Revsbech NP, Jørgensen BB (1986) Microelectrodes: their use
ferent trophic status in the southern Baltic Sea. Mar Ecol in microbial ecology. Adv Microb Ecol 9:293–353
Prog Ser 178:179–191 Revsbech NP, Jørgensen BB, Brix O (1981) Primary pro-
Meyercordt J, Gerbersdorf S, Meyer-Reil LA (1999) Signifi- duction of microalgae in sediments measured by oxygen
cance of pelagic and benthic primary production in two microprofile, H14CO3-fixation, and oxygen exchange
shallow coastal lagoons of different degrees of eutrophica- methods. Limnol Oceanogr 26:717–730
tion in the southern Baltic Sea. Aquat Microb Ecol 20: Revsbech NP, Jørgensen BB, Blackburn TH, Cohen Y (1983)
273–284 Microelectrode studies of the photosynthesis and O2,
Meyer-Reil LA (1994) Microbial life in sedimenatry biofilms — H2S and pH profiles of a microbial mat. Limnol Oceanogr
the challenge to microbial ecologists. Mar Ecol Prog Ser 28:1062–1074
112:303–311 Rieling T (1999) Remineralisation organischen Materials in
Meyer-Reil LA, Neudörfer F (1998) Structure and function of Boddengewässern Mecklenburg-Vorpommerns unter be-
photoheterotrophic biofilms along a gradient of eutrophi- sonderer Berücksichtigung der Bedeutung von Partikeln
cation in a coastal inlet of the southern Baltic Sea. Pro- und Aggregaten. PhD dissertation, Universität Greifswald
ceedings of the Workshop on the 4th and 5th December Rieling T, Gerbersdorf S, Stodian I, Black HJ, Dahlke S,
1997 at the UFZ Centre for Environmental Research Köster M, Meyercordt J, Meyer-Reil LA (2000) Benthic
Leipzig-Halle. In: Becker PM (ed) Microbiology of microbial decomposition of organic matter and nutrient
polluted aquatic ecosystems. UFZ-Bericht 10, Leipzig, fluxes at the sediment –water interface in a shallow coastal
p 199–200 inlet of the southern Baltic Sea (Nordrügensche Bodden).
Miller DC, Geider RJ, MacIntyre HL (1996) Microphyto- In: Flemming BW, Delafontaine MT, Liebezeit G (eds)
benthos: the ecological role of the ‘Secret Garden’ of Muddy coast dynamics and resource management. Proc
unvegetated, shallow-water marine habitats. II. Role in Mar Sci Vol 2. Elsevier Science BV, Amsterdam,
sediment stability and shallow-water food webs. Estuaries p 175–184
19:202–212 Rizzo WM (1990) Nutrient exchange between the water
Mills DK, Wilkinson M (1986) Photosynthesis and light in column and a subtidal benthic microalgal community.
estuarine benthic microalgae. Bot Mar 29:125–129 Estuaries 13:219–226
Neudörfer F, Meyer-Reil LA (1998) Kleinräumige Bestim- Rizzo WM, Lackey GJ, Christian RR (1992) Significance of
mung respiratorischer und photosynthetischer Prozesse euphotic, subtidal sediments to oxygen and nutrient
mit Sauerstoffmikroelektroden in Sedimenten. In: Ver- cycling in a temperate estuary. Mar Ecol Prog Ser 86:51–61
einigung für Allgemeine und Angewandte Mikrobiologie Robinson DH, Arrigo KR, Iturriaga R, Sullivan CW (1995)
(VAAM) (eds) Mikrobiologische Charakterisierung aqua- Microalgal light-harvesting in extreme low-light environ-
tischer Sedimente, Methodensammlung. Oldenbourg ments in McMurdo Sound, Antarctica. J Phycol 31:508–520
Verlag, Wien, p 245–260 Sakshaug E, Bricaud A, Dandonneau Y, Falkowski PG and
Nielsen LP, Christensen PB, Revsbech NP, Sørensen J (1990) 5 others (1997) Parameters of photosynthesis: definitions,
Denitrification and photosynthesis in stream sediment theory and interpretation of results. J Plankton Res 19:
studied with microsensor and whole-core techniques. 1637–1670
Limnol Oceanogr 35:1135–1144 Schiewer U (1998) 30 years’ eutrophication in shallow
Oren A, Kühl M, Karsten U (1995) An endoevaporitic micro- brackish waters — lessons to be learned. Hydrobiologia
bial mat within a gypsum crust: zonation of phototrophs, 363:73–79
photopigments, and light penetration. Mar Ecol Prog Ser Schlungbaum G, Baudler H, Nausch G (1994) Die Darss-Zing-
51:151–159 ster Boddenkette — ein typisches Flachwasserästuar an
Pankow H (1990) Ostsee-Algenflora. VEB Gustav Fischer, der südlichen Ostseeküste. Rostock Meeresbiol Beitr 2:
Jena 5–26
Pickney J, Zingmark RG (1991) Effects of tidal stage and sun Schnese W (1973) Untersuchungen zur Produktionsbiologie
angles on intertidal benthic microalgal productivity. Mar des Greifswalder Boddens (südliche Ostsee). I. Die Hydro-
198 Aquat Microb Ecol 41: 181–198, 2005
graphie: Salzgehalt, Sauerstoffgehalt, Temperatur und shore marine sediments. Limnol Oceanogr 27:552–556
Sestongehalt. Wiss Z Univ Rostock Math-Naturwiss Reihe Underwood GJC, Boulcott M, Raines CA, Waldron K (2004)
22:629–639 Environmental effects on exopolymer production by
Schubert H, Sagert S, Forster RM (2001) Evaluation of the marine benthic diatoms: dynamics, changes in composi-
different levels of variability in the underwater light field tion, and pathways of production. J Phycol 40:293–304
of a shallow estuary. Helgoländer Wiss Meeresunters 55: Walsby AE (1997) Numerical integration of phytoplankton
12–22 photosynthesis through time and depth in a water column.
Shaffer GP, Onuf CP (1983) An analysis of factors influencing New Phytol 136:189–209
the primary production of the benthic microflora in a Wasmund N (1986) Ecology and bioproduction in the micro-
southern California lagoon. Neth J Sea Res 17:126–144 phytobenthos of the chain of shallow inlets (Boddens)
Sommer U (1994) Planktologie. Springer-Verlag, Berlin south of the Darss-Zingst Peninsula (Southern Baltic Sea).
Sommer U (1998) Biologische Meereskunde. Springer-Verlag, Int Rev Gesamten Hydrobiol 71:153–178
Berlin Wasmund N (1990) Characteristics of phytoplankton in
Stodian I, Gerbersdorf S, Rieling T, Black HJ, Köster M, Meyer- brackish waters of different trophic levels. Limnologica 20:
Reil LA (2000) Geochemical investigations of iron and man- 47–51
ganese in coastal sediments of the southern Baltic Sea. In: Wasmund N, Kell V (1991) Characterization of brackish
Flemming BW, Delafontaine MT, Liebezeit G (eds) Muddy coastal waters of different trophic levels by means of
coasts dynamics and resource management. Proc Mar Sci, phytoplankton biomass and primary production. Int Rev
Vol 2. Elsevier Science BV, Amsterdam, p 149–160 Gesamten Hydrobiol 76:361–370
Sundbäck K, Snoeijs P (1991) Effects of nutrient enrichment Wasmund N, Schiewer U (1994) Überblick zur Ökologie und
on microalgal community composition in a coastal shal- Produktionsbiologie des Phytoplanktons der Darß-Zing-
low-water sediment system: an experimental study. Bot ster Boddenkette (südliche Ostsee). Rostock Meeresbiol
Mar 34:341–358 Beitr 2:41–60
Sundbäck K, Enoksson V, Granéli W, Pettersson K (1991) Webb WL, Newton M, Starr D (1974) Carbon dioxide ex-
Influence of sublittoral microphytobenthos on the oxygen change of Alnus rubra: a mathematical model. Oecologia
and nutrient flux between sediment and water: a labora- 17:281–291
tory continuous-flow study. Mar Ecol Prog Ser 74:263–279 Whitney DE, Darley WM (1983) Effect of light intensity upon
Täuscher L (1976) Ökologische Untersuchungen am Mikro- salt marsh benthic microalgal photosynthesis. Mar Biol 75:
phytobenthos im Zingster Strom der Darß-Zingster 249–252
Boddenkette (südliche Ostsee). MS thesis, Universität Wiltshire KH (1992) The influence of microphytobenthos on
Rostock oxygen and nutrient fluxes between eulittoral sediments
Teubner J (1989) Quantitative und qualitative Erfassung sub- and associated water phases in the Elbe Estuary. In:
merser Makrophyten 1986/87— Luftbildanalysen. MS Colombo G, Ferrari I, Ceccherelli VU, Rossi R (eds) Proc
thesis, Universität Rostock 25th Eur Mar Biol Symp. Olsen & Olsen, Fredensborg,
Ullman WJ, Aller RC (1982) Diffusion coefficients in near- p 63–70
Editorial responsibility: Kevin Carman, Submitted: January 16, 2004; Accepted: August 7, 2005
Baton Rouge, Louisiana, USA Proofs received from author(s): November 4, 2005