Aquatic Botany 84 (2006) 294–300
www.elsevier.com/locate/aquabot
Increased CO2 in the water around Littorella uniflora raises
the sediment O2 concentration
Troels Andersen a, Frede Ø. Andersen a,*, Ole Pedersen b
b
a
Institute of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense, Denmark
Freshwater Biological Laboratory, University of Copenhagen, Helsingørsgade 51, 3400 Hillerød, Denmark
Received 23 February 2005; received in revised form 17 October 2005; accepted 21 November 2005
Abstract
In the present study, we set up laboratory experiments with the isoetid plant Littorella uniflora to test whether higher water column CO2
concentrations affect (1) O2 concentrations in leaves and sediment, and (2) nutrient dynamics in the porewater. The experiments showed that at
175 mM CO2 in the water column, which is 10-fold atmospheric equilibrium, a higher biomass of L. uniflora developed (from 302 51 to
390 86 g dry wt m 2) and there were higher O2 concentrations in the leaves (from 120 up to 160% of air saturation) and in the porewater of the
sediment (1.7-fold higher). The O2 concentration in particular increased in the upper 10–30 mm of the sediment at the elevated CO2 concentrations.
The increase in biomass of L. uniflora mostly derived from a significant increase in the leaf biomass (from 97 14 to 137 21 g DW m 2), while
root biomass at high CO2 (253 82 g dry wt m 2) was similar to that of plants growing at low CO2 (205 40 g dry wt m 2). This implied that the
increase in O2 concentration in the sediment was a result of increased O2 production in the leaves rather than of increased root biomass. Porewater
samples from three sediment depths (20, 70 and 120 mm) showed reduced NO3 concentrations at high CO2 concentration, especially at 20 mm
depth layer (mean values for low CO2 ranged from 25 to 60 mM while they were below 25 mM at high CO2), presumably as a result of uptake by L.
uniflora. NH4+ concentrations increased with depth (from nearly 0 up to 100 mM) but were not significantly related to the CO2 concentration. The
PO43 concentrations were low (less than 0.5 mM) and similar at both low and high CO2 treatments at all three depths. The study showed that
photosynthesis of L. uniflora is limited by CO2 at ambient concentrations and that higher CO2 concentrations result in higher O2 release to the
sediment which is important for the cycling and retention of nutrients in sediments of oligotrophic softwater lakes.
# 2005 Elsevier B.V. All rights reserved.
Keywords: Littorella uniflora; Softwater lakes; Increasing atmospheric CO2; Isoetids; Oxygen; Sediment
1. Introduction
In North America and Northern Europe, the littoral zone of
oligotrophic softwater lakes is often inhabited by isoetids.
Isoetids are small slow-growing evergreen perennials all
exhibiting the same growth form characterized by short stiff
leaves arranged in a rosette (Den Hartog and Segal, 1964).
These plants are known to rely primarily on sediment-derived
CO2 for their photosynthesis (e.g. up to 100% for Lobelia
dortmanna, Sand-Jensen and Søndergaard, 1979). Because
CO2 concentrations in the sediment usually are several fold
higher than the concentration of CO2 in the water column
(Wium-Andersen and Andersen, 1972) no effects of rising CO2
* Corresponding author. Tel.: +45 6550 2607; fax: +45 6593 0457.
E-mail address: [email protected] (F.Ø. Andersen).
0304-3770/$ – see front matter # 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquabot.2005.11.006
have been anticipated for this group of aquatic plants (Bowes,
1993). However, a recent study has clearly shown that for
Littorella uniflora, a significant growth response to increased
availability of CO2 in the water column may be expected
(Andersen et al., 2005). When the CO2 concentration in the
water is increased, a shift from a preferential utilization of
sediment-CO2 to a higher uptake of CO2 from the water column
by the leaves is likely (Søndergaard and Sand-Jensen, 1979).
The structure of the isoetids with air lacunae from the leaves
to the roots allows an efficient transport of both CO2 and O2.
Some isoetid species have been shown to release nearly 100%
of the O2 produced by photosynthesis from the roots. This
plant-mediated flux of O2 to the isoetid vegetated sediments is
several fold larger than the diffusive flux to the sediment via the
sediment–water interphase (Sand-Jensen and Prahl, 1982). Of
the O2 produced in light by L. uniflora, 23–50% is lost via the
roots (Sand-Jensen et al., 1982, Roelofs et al., 1984, Robe and
T. Andersen et al. / Aquatic Botany 84 (2006) 294–300
Griffiths, 1990), while non-isoetids only loose 4% (SandJensen et al., 1982). Hence, because of the low organic content
of oligotrophic lake sediments at the shallow part of the littoral
zone and the high input of O2 from the roots of the isoetids,
these sediments are usually oxidized throughout the rhizosphere (Pedersen et al., 1995).
The lower part of the range of free CO2 concentrations in the
porewater of typical isoetid vegetated sediments is below the
level necessary to saturate the photosynthesis in L. uniflora
(range 1–3 mM free CO2, Sand-Jensen and Søndergaard,
1979). It is therefore likely that higher concentrations of free
CO2 will enhance the photosynthesis in L. uniflora which
subsequently may increase the O2 concentrations in the
sediment. In addition, a long-term increase in biomass of
L. uniflora at higher CO2 concentrations (Andersen et al., 2005)
may further increase the transport of O2 to the roots.
Increased radial fluxes of O2 from the roots to the
rhizosphere may have great impact on the biogeochemical
processes of the sediment. For instance, the O2 release may
stimulate nitrification (Christensen and Sørensen, 1986;
Risgaard-Petersen and Jensen, 1997), and increase the binding
of phosphate (PO43 ) to oxyhydroxy-forms of iron (Fe3+) and
manganese (Mn4+) (Christensen and Andersen, 1996). If the O2
release to the sediment increases, an increased rate of
nitrification resulting in more available nitrate (NO3 ) for
the plants is anticipated. Furthermore, reduced diffusive fluxes
of ammonium (NH4+) and PO43 from the sediment to the
water column may also occur. Root release of O2 also allows
aerobic metabolism by microorganisms.
In the present study, we set up laboratory experiments with
L. uniflora vegetation in cores where the water column CO2
could be manipulated in order to test whether higher water
column CO2 concentrations affect: (1) O2 concentrations in
leaves of L. uniflora and in the sediment, and (2) nutrient
dynamics in the sediment.
2. Material and methods
Sediment cores (inner diameter: 114 mm, height: 400 mm)
with Littorella uniflora (L.) were collected in Lake Hampen,
Denmark in May 2004. The height of the sediment in the cores
was approximately 250 mm with a water column of 100 mm.
Detritus and epiphytic algae trapped in the cores were removed
before the cores were placed at 15 8C in large tanks (75 L) with
filtered water from Lake Hampen (mean alkalinity was
0.34 meq L 1, mean total N was lower than 30 mM and mean
total P was lower than 0.6 mM). Aquarium pumps were used to
mix the water in the tanks as well as the water columns in the
cores. Five cores were set up in a tank with low CO2
concentration (17 mM) and similarly five cores in a tank with
high CO2 concentration (175 mM). Low CO2 concentration was
obtained by bubbling the water with atmospheric air (pH 7.7),
whereas high CO2 concentration was obtained by adjusting pH
to 6.7 (0.05 pH unit) by adding gaseous CO2 to the water.
Consequently, low CO2 and high CO2 treatments differed by 1
pH unit in the water column. However, this is less than the
natural pH differences between water and porewater in the
295
sediment and we assume that this will not influence
photosynthesis and/or growth. The CO2 addition was regulated
by a pH controlling system (a pH electrode from Radiometer in
Denmark, connected to a pH-controller, model Alpha from
Dupla in Germany) coupled to a magnetic valve through which
CO2 was provided from a gas cylinder as described by
Andersen and Pedersen (2002). All cores received the same
irradiance (230 mmol photons m 2 s 1) from high-pressure Na
lamps (12 h light/dark).
Two cores, similar to the 10 cores used in the experiment,
were harvested initially. The plants from the two cores were
counted and separated into leaves and roots (the small rhizome
part were included in the root fractions) and dried for 24 h at
105 8C to determine the initial shoot density and biomass of
leaves and roots.
Samples of lake water and porewater of the L. uniflora
vegetated sediment (20, 70 and 120 mm depth) for measurements of O2 concentration, pH and alkalinity were taken when
the sediment cores were collected in Lake Hampen. Porewater
samples were taken with a syringe connected to a metal tube
(inner diameter 2 mm), which had three holes (diameter
0.5 mm) near the sealed tip. Twenty mL were sampled from
each sampling depth at three different places in the L. uniflora
vegetation. The O2 concentration was measured immediately
after sampling with an oxygen microelectrode (Unisense OX500, Denmark), pH was measured with a combined pH
electrode (Radiometer, Denmark), and alkalinity was determined in the laboratory by Gran-titration with 0.1 mM HCl
(Mackereth et al., 1978). The CO2 concentration in the samples
was calculated from pH, alkalinity and dissociation constants
corrected for ionic strength and temperature using the equations
in Maberly (1996).
After 1 month of growth in the laboratory, O2 was measured
in water, leaves and sediment by O2 microelectrodes (Unisense
OX-50 or OX-500, Denmark). The O2 electrode was connected
to a picoamperemeter (Unisense PA2000, Denmark), from
which data in millivolts was logged by a computer using an a/d
converter (ADC16, PicoTech, England). During measurements,
each core was isolated in a separate tank to minimize
disturbances. Air stones were placed directly in the water
phase of the cores. Low CO2 cores received atmospheric air,
and the high CO2 cores were supplied with a mixture of
atmospheric air and CO2 (Mass Flow Controller, Brooks 5850
TR Series, The Netherlands). This provided O2 conditions
(100% atmospheric equilibrium) in the water phases of high
CO2 cores similar to low CO2 cores and about 175 mM of free
CO2 similar to high CO2 treatments elsewhere.
In leaf O2 measurements, the tip of the microelectrode was
placed approximately in the centre of the leaf. At the same time,
microelectrodes monitored O2 concentrations in the water
phases of the cores to ensure that the O2 concentration in the
water phase remained in equilibrium with the atmosphere. O2
concentrations were logged as an average once every minute for
at least a full light/dark cycle.
Finally, O2 concentrations were measured in profiles from
the water phase and down to a maximum depth of 48 mm in
both low CO2 and high CO2 cores. The microelectrode was
296
T. Andersen et al. / Aquatic Botany 84 (2006) 294–300
advanced in 1 mm steps by a micro manipulator. After 30 s, the
signal was sampled, and the microelectrode moved deeper into
the sediment. Four replicates of O2 profiles were recorded in
three cores from each treatment, resulting in 12 O2 profiles from
both low CO2 and high CO2 cores, respectively.
Porewater samples (12 mL) for inorganic N and P were
taken six-times during the 53-day experiment in three depths
(20, 70 and 120 mm) from a metal tube (inner diameter 2 mm)
horizontally inserted through the core. The tube was perforated
with tiny holes over 100 mm length allowing a sample from a
cylindrical sediment column around the tube to be taken. The
layer around the tube, from which the sediment porewater was
drawn, was about 9 mm thick, assuming a sediment porosity of
50%. The samples were filtered through glass fibre filters
(Whatman GF/C) and samples for NO3 and NH4+ were stored
frozen, while samples for PO43 were preserved with 2 M
H2SO4 (75 mL/12 mL sample) and stored at 5 8C. The samples
were analysed for the sum of nitrite (NO2 ) and NO3
(hereafter called NO3 since NO2 never exceeded 1% of the
total) by a flow injection analyser (Tecator FIA Star 5012) and
manually for NH4+ (Bower and Holm-Hansen, 1980) and for
PO43 (Koroleff, 1983).
After 53 days of growth, the plants were harvested to
estimate shoot density, number of leaves per plant, leaf
biomass, root biomass, and total plant biomass. Root biomass
was further separated into rhizomes, root parts from 0 to 5 cm
length, and root parts longer than 5 cm. The plant material was
dried for 24 h at 105 8C to determine the biomass.
All data were normal distributed and were subsequently
statistically analysed for significant effects of CO2 by Student’s
t-test, analysis of variance (ANOVA) and Tukey HSD-test.
higher than in leaves of plants at low CO2. In plants at high CO2,
the maximum O2 concentration in the presented dataset was
160% of air saturation and the concentration was consistently
higher throughout the light period compared to plants at low
CO2. The O2 concentration in leaves decreased after 6–7 h at
both low CO2 and high CO2 due to CO2 substrate limitation.
However, the O2 concentration decreased more slowly at high
CO2 than at low CO2 (Fig. 1). During darkness, respiration and
loss of O2 from the roots to the sediment led to an initial abrupt
decline in lacunal O2 concentrations but near steady-state
conditions were reached after 4–5 h at about 60–70% of air
saturation.
The higher O2 concentration in the leaves of plants at high
CO2 was accompanied by increased O2 concentrations in the
porewater. Both during light and darkness, the O2 concentration
in the sediment was consistently higher at high CO2 than at low
CO2 (data not shown). The O2 profiles during steady-state in
light from the sediment surface and down to 48 mm depth
showed significantly higher O2 concentrations in sediments at
high CO2 (Fig. 2). The O2 concentrations at 2 mm above the
sediment and in the top 4 mm of the sediment were similar at
low and high CO2 and agreed well with the observed growth of
benthic microalgae on the sediment surface of all cores. The O2
concentrations remained high in sediments at high CO2 and
decreased only moderately down to 30 mm depth, while the O2
3. Results
Upon illumination, photosynthesis in L. uniflora immediately responded and the O2 evolution caused high O2
concentrations in the leaf lacunae (Fig. 1). The O2 concentrations in leaves of L. uniflora at high CO2 in light tended to be
Fig. 1. O2 concentrations in leaves and water from low CO2 and high CO2 in a
typical paired dataset. Data were normalized to low CO2 in light and showed the
following pattern: low CO2 in darkness 0.37 0.03, low CO2 in light
1.0 0.00, high CO2 in darkness 0.42 0.02, and high CO2 in light
1.11 0.04 (mean S.D., n = 2–4).
Fig. 2. O2 profiles in sediment cores treated with low and high CO2 concentration in the water phase. Each curve represents an average of three cores, in
which four profiles were measured during steady-state in light. The O2 concentrations at high CO2 were significantly higher than at low CO2 (P < 0.001).
The coefficient of variance between the three replicates was 27.1% for high CO2
profiles and 26.1% for low CO2 profiles.
T. Andersen et al. / Aquatic Botany 84 (2006) 294–300
concentrations in sediments at low CO2 decreased down to a
depth of 12 mm to a local minimum of 65% of air saturation
(Fig. 2). For all profiles both at low and high CO2, there was a
peak in O2 concentration in the depth of 20–30 mm. At depths
below 30 mm, the O2 concentrations decreased to 50% of air
saturation at low CO2 but only to about 75% at high CO2
(Fig. 2).
The in situ samples of the water just above the sediment and
of the porewater in 20, 70 and 120 mm depth of the L. uniflora
vegetated bed in Lake Hampen showed almost similar O2
concentrations (Fig. 3) as observed at low CO2 in the laboratory
(Fig. 2). O2 concentrations in the lake water 20 mm above the
sediment was close to air saturation, and in 20 mm depth, the O2
concentration was approximately 75% of air saturation. In 70
and 120 mm depth, O2 concentrations were just above and
below 25% of air saturation, respectively.
The alkalinity in Lake Hampen decreased from the water
phase to the lowest measured value at 20 mm depth (Fig. 3). In
70 mm depth, alkalinity was higher than in the water phase, and
the alkalinity increased further to almost 0.5 meq L 1 at
120 mm depth. pH was higher in the water phase than in the
porewater where pH values were uniform and about 6.5
regardless of depth (Fig. 3). pH in the experimental cores
increased with time from 6.2 up to between 6.7 and 7.0, with the
297
highest values in 120 mm depth (data not shown). Even though
pH was experimentally lowered with 1 unit in the water phase at
high CO2, pH in the sediment was in general only 0.15 units
lower in the sediment at high CO2 than in sediment at low CO2
(data not shown). The concentration of free CO2 in the samples
from Lake Hampen increased almost linearly from the water
phase (0.04 mM) to approximately 0.35 mM at 120 mm depth
(Fig. 3).
The NO3 concentration at 20 mm depth at high CO2 was
significantly lower (P < 0.01) than the concentration at low
CO2 depth, and the concentration at high CO2 decreased during
the experimental period from 21.7 to 3.9 mM (Fig. 4). At 70
and 120 mm depths, the NO3 concentrations were not
significantly different at high CO2 and low CO2. NH4+
concentrations were not significantly different in the two CO2
treatments, but only a tendency for reduced NH4+ concentration at high CO2 in 20 mm depth was observed (Fig. 4). Over
time, the NH4+ concentrations increased during the early part
of the experiment until a maximum was reached after
approximately 20 days, after which the concentrations
decreased again (Fig. 4). The NH4+ concentrations increased
with sediment depth. We observed no significant differences in
porewater PO43 concentrations between low and high CO2
treatments (Fig. 4).
Fig. 3. O2 concentrations, pH, CO2 concentrations and alkalinity in sediment porewater in Lake Hampen at the collection of the vegetated cores (mean S.E., n = 3).
298
T. Andersen et al. / Aquatic Botany 84 (2006) 294–300
Fig. 4. Changes with time in inorganic N and P concentrations in the porewater at three sediment depths. The sediment were treated with either low or high CO2
concentration in the water phase (mean S.E., n = 5). NO3 concentrations at high CO2 were significantly lower than at low CO2 in 20 mm depth (P < 0.01).
4. Discussion
4.1. Limitation by CO2
It has been shown that CO2 concentrations above 1.5 mM
around the leaves are necessary to saturate the photosynthesis
of L. uniflora when measured on abscised leaves (Sand-Jensen,
1987). Nevertheless, the high CO2 concentration in the water
column in the present study (150 mM) was adequate to
stimulate the photosynthetic O2 evolution markedly. In the
sediment of Lake Hampen, CO2 concentrations are in the lower
end of the typical range for Lobelia lakes. Hence, the
photosynthesis of L. uniflora is obviously limited by CO2 at
ambient concentrations in Lake Hampen and therefore,
addition of CO2 caused the higher O2 production observed
in our study.
Elevated CO2 concentrations also resulted in higher plant
densities, leaf biomass and total biomass (Table 1). In the
field, L. uniflora often has high densities of 5000–
7500 plants m 2, and the biomass can exceed 100 g dry wt
m 2 (Sand-Jensen and Søndergaard, 1979, 1997). In the
present study, both plant density and biomass estimates for
high CO2 treatments were clearly higher, and the density
almost doubled compared to the initial values. In the present
study, higher temperature and irradiance under the laboratory conditions are most likely causing the increase in
biomass and shoot density also at low CO2 treatments. The
higher temperature is stimulating the decomposition of
organic matter in the sediment leading to higher nutrient
concentrations. This may, in turn, explain the observed
higher leaf:root ratio both at low and high CO2 treatments
(Table 1).
T. Andersen et al. / Aquatic Botany 84 (2006) 294–300
299
Table 1
Biomass, leaf:root ratio, plant density and number of leaves for L. uniflora at collection of the cores in Lake Hampen (initial) and at the end of the experiment (low
CO2 and high CO2)
Variable
Initial
Low CO2
High CO2
2
Biomass (g dry wt m )
Plants
Leaves
Roots
Rhizome
0–5 cm
>5 cm
Leaf:root ratio
Plant density (m 2)
No. of leaves (plant 1)
342 65 a
46 9a
302 51a
97 14b
390 86a
137 21c
295 56 a
–
–
–
205 40a
80 20a
115 21a
10 3a
253 82a
90 42a
150 40a
14 5a
0.16 0.00a
4519 1508a
–
0.48 0.06b
8673 2072b
4.47 0.29a
0.57 0.15b
8693 1128b
4.51 0.24a
Mean values and standard deviations are given. Different letters in superscript indicate significant differences.
4.2. Oxygen dynamics
Apparently, in our experiment, L. uniflora had maximum root
density between 20 and 30 mm in the sediment since the O2
concentration increased abruptly at this depth. On the other hand,
at the depth of maximum root density (normally 10–20 mm into
the sediment, Sand-Jensen and Søndergaard, 1997) a substantial
O2 consumption by plant and microbial biomass takes place at
night. Deeper into the sediment, the microbial O2 consumption
rates are much lower due to the lack of degradable organic
substrates, and the O2 amplitudes between day and night are
much dampened because of lower root density and release rates
of O2 (Pedersen et al., 1995, Sand-Jensen and Søndergaard,
1997). All O2 profiles in the present study were measured in light
and showed an O2 peak at the sediment surface due to the
photosynthesis of benthic microalgae (Pedersen et al., 1995).
When measuring deeper in the sediment, the profiles had the
same shape at low and high CO2 but with higher absolute levels at
high CO2. Hence, it seems that the higher O2 production in leaves
at high CO2 also translates into a higher root-release of O2.
4.3. Nutrient dynamics
In the present study, NO3 concentrations were highest in
the top layer (20 mm depth). Here, the levels were comparable
to studies by Olsen and Andersen (1994), while Roelofs (1983)
found several fold higher concentrations in Dutch lake
sediments with L. uniflora. The relatively high NO3
concentrations at 20 mm depth indicate a high nitrification
rate because the majority of NO3 uptake by the roots also
occurs around this depth. The significantly higher NO3
concentrations at 20 mm depth at low CO2 than at high CO2
were most likely due to lower uptake of NO3 by the lower
plants at low CO2. Deeper in the sediment, NO3 was depleted,
perhaps due to a decreased nitrification combined with an
increased denitrification (Olsen and Andersen, 1994).
A reduction in the NH4+ concentration was observed at high
CO2 at 20 mm depth which coincided with a significantly higher
O2 concentration. The low NH4+ concentration was therefore
probably caused by combined effects of plant uptake and
nitrification. Previous studies have shown insignificant release of
NH4+ from this type of sediment (Andersen et al., 2005). Maxima
of NH4+ concentrations developed over time (especially at 70 and
120 mm depth after 10–25 days). These maxima were likely a
result of mineralization of labile organic material. Field
measurements of NH4+ in L. uniflora sediments usually show
a decreasing concentration with depth (Olsen and Andersen,
1994, Nielsen and Andersen, 2005). In contrast, increasing NH4+
concentrations with depth were observed in the present
experiment. The NH4+ gradient, however, decreased with time
after the maxima, probably because of an upward diffusion and
nitrification followed by NO3 uptake by the plants. The NH4+
concentrations in our experiment were within the range
(normally 0–50 mM) found in L. uniflora sediments in three
Danish lakes (Olsen and Andersen, 1994, Nielsen and Andersen,
2005), but low compared to Dutch lakes which had a mean
concentration of 267 mM (Roelofs, 1983). This difference may
be due to the low organic content of the sediment in the Danish
lakes and a high root-mediated O2 release.
Inorganic P typically limits plant growth in Lobelia lakes
(Moeller, 1978) and dissolved P is extremely low (<1 mM) in
the porewater of the oxic L. uniflora rhizosphere (e.g.
Christensen et al., 1998, Nielsen and Andersen, 2005). Thus,
the low PO43 concentrations in the present study (<0.5 mM at
all three sediment depths) during the entire experimental period
were in accordance with the previous studies. Although the
NH4+ concentrations indicated a mineralization in the deeper
parts of the sediment, this did not lead to increased PO43
concentrations, probably due to plant uptake and because
PO43 is bound to especially iron oxyhydroxides in the
oxidized sediment (e.g. Christensen and Andersen, 1996).
Acknowledgement
This study was supported by a grant (No. 55-00-0337) from
the National Science Council of Denmark to O. Pedersen and
F.Ø. Andersen and an ASEM-DUO Fellowship to T. Andersen.
References
Andersen, T., Pedersen, O., 2002. Interactions between light and CO2 enhance
the growth of Riccia fluitans. Hydrobiologia 477, 163–170.
300
T. Andersen et al. / Aquatic Botany 84 (2006) 294–300
Andersen, T., Pedersen, O., Andersen, F.Ø., 2005. Nutrient concentrations in a
Littorella uniflora community at higher CO2 concentrations and reduced
light intensities. Freshwater Biol. 50, 1178–1189.
Bower, C.E., Holm-Hansen, T., 1980. A salicylate-hypochlorite method for
determining ammonia in seawater. Can. J. Fish. Aquat. Sci. 37, 798.
Bowes, G., 1993. Facing the inevitable: plants and increasing atmospheric CO2.
Annu. Rev. Plant Physiol. Plant Mol. Biol. 44, 309–329.
Christensen, K.K., Andersen, F.Ø., 1996. Influence of Littorella uniflora on
phosphorus retention in sediment supplied with artificial porewater. Aquat.
Bot. 55, 183–197.
Christensen, K.K., Jensen, H.S., Andersen, F.Ø., Wigand, C., Holmer, M., 1998.
Interferences between root plaque formation and phosphorus availability for
isoetids in sediments of oligotrophic lakes. Biogeochemistry 43, 107–128.
Christensen, P.B., Sørensen, J., 1986. Temporal variation of denitrification
activity in plant-covered littoral sediment from Lake Hampen, Denmark.
Appl. Environ. Mic. 51, 1174–1179.
Den Hartog, C., Segal, S., 1964. A new classification of the water-plant
communities. Acta Bot. Neerl. 13, 367–393.
Koroleff, F., 1983. Determination of phosphorus. In: Grasshof, K., Erhardt, M.,
Kremling, K. (Eds.), Method of seawater analysis. 2nd ed. Verlag Chemie,
Weinheim.
Maberly, S.C., 1996. Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshwater Biol. 35, 579–598.
Mackereth, F.J.H., Heron, J., Talling, J.F., 1978. Water Analysis: Some Revised
Methods For Limnologists. Freshwater Biological Association. Ambleside,
United Kingdom.
Moeller, R., 1978. Seasonal changes in biomass, tissue chemistry, and net
production of the evergreen hydrophyte, Lobelia dortmanna. Can. J. Bot.
56, 1425–1433.
Nielsen, K.B., Andersen, F.Ø., 2005. Interactions of the macrophyte Littorella
uniflora with sediment phosphate fractions in three Danish oligotrophic
lakes. In: Serrano, L., Golterman, H.L. (Eds.), Phosphorus in Sediments.
Proceedings of the 4th International Symposium on Phosphate in Sediments. Backhuys Publishers, Leiden, pp. 173–183.
Olsen, K.R., Andersen, F.Ø., 1994. Nutrient cycling in shallow, oligotrophic
Lake Kvie, Denmark. I. Effects of isoetids on the exchange of nitrogen
between sediment and water. Hydrobiologia 275/276, 255–265.
Pedersen, O., Sand-Jensen, K., Revsbech, N.P., 1995. Diel pulses of O2 and CO2
in sandy lake sediments inhabited by Lobelia dortmanna. Ecology 76,
1536–1545.
Risgaard-Petersen, N., Jensen, K., 1997. Nitrification and denitrification in the
rhizosphere of the aquatic macrophyte Lobelia dortmanna L. Limnol.
Oceanogr. 42, 529–537.
Robe, W.E., Griffiths, H., 1990. Photosynthesis of Littorella uniflora under two
par regimes: C3 and CAM gas exchange and the regulation of internal CO2
and O2 concentrations. Oecologia 85, 128–136.
Roelofs, J.G.M., 1983. Impact of acidification and eutrofication on macrophyte
communities in soft waters in the Netherlands. 1. Field observations. Aquat.
Bot. 17, 139–155.
Roelofs, J.G.M., Schuurkes, J.A.A.R., Smiths, A.J.M., 1984. Impact of acidification and eutrophication on macrophyte communities in soft waters. II.
Experimental studies. Aquat. Bot. 18, 389–411.
Sand-Jensen, K., 1987. Environmental control of bicarbonate use among
freshwater and marine macrophytes. In: Crawford, R.M.M., Wada, K.,
Hiraki, A. (Eds.), Plant Life in Aquatic and Amphibious Habitats 99113. Special publications series of the British Ecological Society (no. 5).
Blackwell Scientific Publications, Oxford, United Kingdom.
Sand-Jensen, K., Prahl, C., 1982. Oxygen exchange with the lacunae and across
leaves and roots of the submerged vascular macrophyte, Lobelia dortmanna.
New Phytol. 91, 103–120.
Sand-Jensen, K., Søndergaard, M., 1979. Distribution and quantitative
development of aquatic macrophytes in relation to sediment characteristics in oligotrophic Lake Kalgaard, Denmark. Freshwater Biol. 9, 1–
11.
Sand-Jensen, K., Søndergaard, M., 1997. Plants and environmental conditions
in Danish Lobelia-lakes. In: Sand-Jensen, K., Pedersen, O. (Eds.), Freshwater Biology. GEC GAD, Copenhagen, Denmark, pp. 54–73.
Sand-Jensen, K., Prahl, C., Stokholm, H., 1982. Oxygen release from roots of
submerged aquatic macrophytes. Oikos 38, 349–354.
Søndergaard, M., Sand-Jensen, K., 1979. Carbon uptake by leaves and roots of
Littorella uniflora. Aquat. Bot. 6, 1–12.
Wium-Andersen, S., Andersen, J.M., 1972. Carbon dioxide content of the
interstitial water in the sediment of Grane Langsø, a Danish Lobelia lake.
Limnol. Oceanogr. 17, 943–947.